Selected Readings In Mammalogy J. Knox Jones, Jr. Sydney Anderson Robert S. Hoffmann Museum of Natural History The University of Kansas 1976 fu QA HA “M, P ct f rd T f 6 a ) SuTHERS, R. A. Comparative echolocation by fishing bats. J. Mamm., 48:79-87, 1967 aes eg SP eae oa ee eee ts AN vil Roserts, M. W., and J. L. WoLFE Social influences on susceptibility to predation in cotton rats. Je Mami. 992560-3(2, 19 (4-21 oe een Pe McCartey, H. Ethological isolation in the cenospecies Peromyscus leucopus, Evolitions, 15:83 1-332) 1964) i) oe 8h Ee ee ee GRODZINSKI, W. Influence of food upon the diurnal activity of small rodents. Pp. 134-140, in Satesn Theriologicum, Czech. Acad. Sci., Prague, OG 2s ee: eee OU ee cA, Ata eeh Dire otek Ie ee Le Bar_Low, G. W. Galapagos sea lions are paternal. Evolution, 28:476-478, 1974 SAMARAS, W. F. Reproductive behavior of the gray whale Eschrichtius robustus, in Baja California. Bull. Southern California Acad. Sci., ge Pro FE Ge: SNS 71: Th acted SRL dA ESTE Bek Meet eee Se EE I Roncsrap, O. J., and J. R. Tester Behavior and maternal relations of young snowshoe hares. We Waldlite: Mgt °35°308-346" 107) ee ee eee SECTION 5—PALEONTOLOGY AND EVOLUTION REED, C. A. The generic allocation of the hominid species habilis as a problem in systematics, Seuth Atrican |. Sci:, 65:3-5,.196/ 2 ZAKRZEWSKI, R. J. Fossil Ondatrini from western North America. J. Mamm., EVN AO NO Ara gee ee Se er ee ee Witson, R. W. Type localities of Cope’s Cretaceous mammals. Proc. South Dakota Acad. Sci., 44:88-90, 1965 Rapinsky, L. B. The adaptive radiation of the phenacodontid condylarths and the origin of the Perissodactyla. Evolution, 20:408-417, 1966 Woon, A. E. Grades and clades among rodents. Evolution, 19:115-130, 1965 NADLER, C. F., R. S. HOFFMANN, and K. R. GREER Chromosomal divergence during evolution of ground squirrel populations (Rodentia: Spermophilus). Syst., Zool., 21 UEOAS he ase 15 Sea) 1 Ree ne NI ave eR Bec C Gutu,ig, R. D. Variability in characters undergoing rapid evolution, an analysis of Microitus molars, Evolution, 19:214.233, 1965 2. 22. 2 ae JAnsxy, L. Evolutionary adaptations of temperature regulation in MatimalsaZ.caleeven, o2:kos-l12, 1967 me sien 0 ee Vili HerrHaus, E. R., P. A. OPLER, and H. G. BAKER Bat activity and pollination of Bauhinia pauletia: plant-pollinator coevolution. Ecology, 55:412-419, 1974... Smit, M. H., R. W. Buessinc, J. L. CArMon, and J. B. GENTRY Coat color and survival of displaced wild and laboratory reared old-field mice. Acta Theriol., 14:1-9, 1969 __- SECTION 6—ZOOGEOGRAPHY AND FAUNAL STUDIES KurtEN, B. Notes on some Pleistocene mammal migrations from the Palaearctic to the Nearctic. Eiszeitalter u. Gegenwart, 14:96-103, 1963 _.. Guitpay, J. E. Pleistocene zoogeography of the lemming, Dicrostonyx. Evolution, 17:194-197, 1963 ____ pasts Koopman, K. F., and P. S. MARTIN Subfossil mammals from the Gémez Farias region and the tropical gradient of eastern Mexico. J. Mamm., 40:1-12, 1959 Brown, J. H. Mammals on mount: aintops: ae were insular biogeogr aoe Amer. Nat., 105:467-478, 1971 | FINDLEY, J. S., and S. ANDERSON Zoogeography of the montane mammals of Colorado. 1 Mamm.. 37:80-82, 1956 - Hansen, R. M., and G. D. Bear Comparison of pocket gophers from alpine, subalpine and shrub- grassland habitats. J. Mamm., 45:638-640, 1964 . 7 Wiuson, D. E. Bat faunas: a trophic comparison. Syst. Zool., 22:14-29, 1973 - HAcMEIER, E. M. A numerical analysis of the distributional patterns of North American mammals. II. Re-evaluation of the provinces. Syst, Zool;,15:279-299. 1966 en ener ae Wison, J. W., II Analytical zoogeography of North American mammals. Evolution, 28:124-140, 1974 - [ireRATURE CITED ...- 2 ix _ 539 547 551 563 _ 575 578 _ 581 _ 597 618 _ 635 SHLECTED READINGS IN MAMMALOGY INTRODUCTION The overall unity of the different fields of science and of other aspects of human experience, or at least their interdependence, is evident in both theory and practice. Nevertheless, this is an age of specialization. The sheer volume of information, the current rate of increase in knowledge, the changing and often elaborate techniques that must be learned, and human limitations all have contributed to the production of specialties. A definition of the specialty of mammalogy as “all scientific study of mam- mals” is too broad, for that definition encompasses, for example, all parts of animal physiology in which any mammal, such as a white rat in the laboratory, may happen to be used. It also would include much of medical practice, because humans are mammals. Generally speaking, those scientists who call themselves mammalogists are interested in the mammal as an animal—as an organism—not just as a specific case of some more general phenomenon, be it the nature of life or the nature of the nerve impulse. For example, a physiolo- gist who is interested in comparative studies between different mammals or in the functicn of a physiological process as an adaptive mechanism may regard himself as a mammalologist. A physiologist who studies one kind of laboratory animal and is interested in explaining a process in terms of progressively sim- pler mechanisms rarely will regard himself as a mammalogist. Both types of study, of course, contribute to biological knowledge. Life is best comprehended in terms of four basic concepts: first, that biology, as all of science, is monistic, assuming one universe in which the same natural laws apply to living and non-living things; second, that life is a dynamic and self-perpetuating process; third, that the patterns of life change with time; finally, that these factors together have resulted in a diversity of living forms. Different branches of biology tend to focus or concentrate on different concepts. Thus, the above four concepts are focal points, respectively, of (1) physiology and biochemistry, (2) ecology, (3) evolutionary biology, and (4) systematic biology. Mammalogy is the study of one systematic group or taxon, the Class Mammalia. Studies emphasizing different aspects of mammalian biology are evident in our section headings and in the specific papers repro- duced. Biology as a whole and mammalogy specifically may be best likened to a woven fabric rather than to a series of compartments. We feel that a unifying conceptual scheme for “mammalogy” lies in the realm of “systematic mammalogy.” This scheme is unifying because it includes the basis for subsequent study and the only meaningful framework for the synthesis of existing knowledge of mammals. On this point, George Gaylord Simpson, in introducing his classic The Principles of Classification and a Classi- fication of Mammals (1945) wrote (Simpson at that time used the term “taxonomy as we use “systematics’ ) : “Taxonomy is at the same time the most elementary and the most inclusive part of zoology, most elementary because animals cannot be discussed or treated in a scientific way until some taxonomy has been achieved, and most inclusive because taxonomy in its various guises and branches eventually gathers together, utilizes, summarizes, and imple- ments everything that is known about animals, whether morphological, physiological, psychological, or ecological.” Knowledge of the identity of any animal studied is essential so that the results may be compared with other knowledge about the same kind of animal and with the same kind of knowledge about different animals. We originally had hoped to develop the history of mammalogy along with our other objectives, but when the hard fact of page limitation was faced, some selections whose chief justification was historical were sacrificed. In the comments beginning each section, some historical information helps place the selections in an understandable framework. To attain variety we have included papers both of restricted and of general scope; for example, papers pertaining to local faunas and continental faunas, to higher classification and infraspecific variation, and to contemporary serum proteins and millions of years of evolution are reproduced here. Every serious student of mammalogy, whether amateur or professional, researcher or compiler, writer or reviewer, artist or teacher, must learn to use the literature. One does not learn all about mammals because that is impossi- ble. One learns what one can, where to look for further information, and, more important, how to evaluate what one finds. Most of the literature on mammals is in technical journals, a few of which are devoted exclusively to mammalogy: JouRNAL or MAmM™MaALocy (USA), MAMMALIA (France), ZEITSCHRIFT FUR SAUGETIERKUNDE (Germany), SAUGE- TIERKUNDLICHE MITTEILUNGEN (Germany), Lurra (Benelux countries), LyNx (Czechoslovakia), AcrA Tuertotocica (Poland), Mamma Review (Great Britain), THertoLocy (USSR), THE JouRNAL OF THE MAMMALOGICAL SOCIETY OF JAPAN, and AUSTRALIAN MAmM™MaAtocy. Also there is the specialized Fouia PRIMATOLOGICA, an international journal of primatology, founded in 1963, and a number of serial publications such as JouRNAL OF WILDLIFE MANAGEMENT, East ArricAN WILDLIFE JOURNAL, BULLETIN OF THE WILDLIFE DisEASE As- SOCIATION, SOUTHWESTERN NATURALIST, and journals issued by various game departments and conservation agencies that may deal in large part, but not exclusively, with mammals. However, much of the published information on mammals, as on most aspects of biology, is widely scattered. About 40 journals include 50 per cent of the current literature, but to cover 70 per cent, at least 150 journals must be consulted. Articles in the JouRNAL oF MAMMALOGY (now approximately 900 pages each year) comprise only about three per cent of all current titles on mammals, for example. Some categories of literature other than journals are books, symposia, transactions of various meetings or groups such as the Transactions of the North American Wildlife and Natural Resources Conference (the 40th was issued in 1975), yearbooks such as the International Zoo Yearbook (the 15th was published in 1975), newsletters such as the Laboratory Primate News- letter, Carnivore Genetics Newsletter, Mammalian Chromosome Newsletter, or Bat Research News, major revisions or compilations of special subjects, bibliographies, and abstracts. The chief bibliographic sources for mammalo- gists are the JouRNAL oF MAmMMALocy, through its lists of Recent Literature, SAUGETIERKUNDLICHE MITTEILUNGEN, through its “Schriftenschau” section, the ZooLocicaL Recorp, published by the Zoological Society of London, Bio- LocicaL Asstracts, and the quarterly Witpire Review that is issued by the US. Fish and Wildlife Service (along with the three collections of WILDLIFE ApsTRACTs—a misnomer because only citations are included—compiled there- from and published in 1954, 1957, and 1964); one especially useful bibliogra- phy to older papers on North American mammals is that compiled by Gill and Coues (in Coues and Allen, 1877). Some individuals and institutions main- tain records in the form of card files, or collections of separates, or both, over many years for special subjects, special geographic areas, or other more gen- eral purposes. It is important for the student to remember that large-scale faunal reports, catalogues, revisionary works, and the like often are valuable as bibliographic sources as well as sources of other information. Some of these reports are mentioned in the introductory remarks to several sections. An individual who delves into the literature on a particular subject usually begins with one or more pertinent recent works and proceeds backward in time by consulting publications cited in the later works or found in other bibliographic sources. An amazing amount of published information on a given subject frequently is available to the person willing to look for it. However, paradoxically, there is often no published record for what one might suppose to be nearly common knowledge. The questioning mind must return to nature when the literature holds no answer, exactly what the authors of papers reproduced in this an- thology have done. A few decades ago only a small number of American colleges and univer- sities offered a formal course in mammalogy, and only since about 1950 have such courses been widely offered. It is not surprising, therefore, that only three textbooks, Cockrum’s Introduction to Mammalogy (1962), Principles in Mam- malogy by Davis and Golley (1963), and Mammalogy by Vaughan (1972) have been published in English. Some instructors use general works such as Recent Mammals of the World, A Synopsis of Families (edited by Anderson and Jones, 1967) or Mammals of the World, a three-volume work by Walker et al. (1964 and subsequent editions) as texts or as references along with other suggested readings. A Manual of Mammalogy by DeBlase and Martin (1974) is another useful reference. Accounts of the mammals of certain states or regions also may be used as texts by persons in those places. Other general works of reference value are Bourliére’s Natural History of Mammals (1954), Young’s The Life of Mammals (1957), Crandall’s Management of Wild Mam- mals in Captivity (1964), the fascicles on mammals in the Traité de Zoologie (edited by Grassé, 1955 and later), and four volumes on mammals in the Encyclopedia of Animal Life (edited by Grzimek, 1972 and later). Two classic general works less readily available are An Introduction to the Study of Mammals, Living and Extinct by Flower and Lydekker (1891) and Mammalia by Beddard (1902) in the Cambridge Natural History series. Compact field guides to the mammals of a few parts of the world are avail- able, such as those of Burt and Grossenheider (1964), Palmer (1954), and Anthony (1928) for parts of North America, Van den Brink (1967) for Europe, Prater (1965) for India, Flint et al. (1965) for the Soviet Union, and Dorst and Dandelot (1970) for the larger mammals of Africa. Morzer-Bruyns’ (1970) field guide to cetaceans is world-wide in scope. The dates in the two preceding paragraphs suggest the recent expansion in the volume of work in mammalogy. Another such measure is membership in The American Society of Mammalogists, which grew from 252 in 1919 to almost 4000 in 1976. Interested persons are invited to apply for member- ship in this society, members of which receive the JOURNAL oF MAMMALOGY. Human medicine, veterinary medicine, animal husbandry, and animal physiology (including much work with a comparatively few species of mam- mals in the laboratory), all preceded mammalogy as separate disciplines deal- ing with mammals. Many of the first mammalogists (as defined here) trained themselves in one of these disciplines and some also practiced in fields other than mammalogy. C. Hart Merriam, who founded the U.S. Biological Survey, studied medicine, as did E. A. Mearns, who wrote on mammals of the Mexican boundary (1907). Harrison Allen wrote much of his first review of North American bats (1864) while on furloughs from duty as a surgeon in the Union army during the Civil War. Mammalogists continue to interact with specialists in the above-mentioned fields to their mutual benefit. Another largely separate but partly overlapping field that flowered slightly later than mammalogy is genetics. We have included no papers on mammalian genetics as such, although the relevance of genetics is evident in some of our selections. The book on Comparative Genetics of Coat Color in Mammals by Searle (1968) contains about 800 references, including some fascinating works on species other than the oft-studied mouse (Mus musculus ). Our six groupings of papers are somewhat arbitrary. Ecology is as closely allied to physiology or zoogeography as to behavior, and anatomy could as well have been placed with development as with physiology. The present arrange- ment as to the sequence of sections and their contents seems to be about as convenient as any other, and that is the extent of our expectations. We imply no hierarchy of subdisciplines. In selecting works to be included here, we have, in addition to the consider- ations already noted, sought papers in which different kinds of mammals were compared, and in which different approaches, styles, and methods of presenta- tion were used. Individual papers often pertain to more than one area of study. In fact, we favored papers that illustrated the relevance of different disciplines and methods of study to each other. Perhaps the reader will be able to ap- preciate our moments of anguish as the final selections were made for this anthology. Our introduction for each section is brief. We hope that our comments aid the reader in considering (1) some historical aspects that make the papers more meaningful, (2) the major areas of study and some major concepts that the papers illustrate, (3) the existence of related literature, to which we can only call attention by citing a few examples, and (4) the continuous transfer of ideas, methods, and results from one worker to another, from one field of science to another, and between science and other fields of human endeavor. SECTION 1—SYSTEMATICS A sound classification provides the necessary framework upon which other information about mammals can be ordered. In order to classify organisms, it first is necessary to assess their similarities and differences; in other words, structures and their functions need to be observed, described, and compared, and taxa need to be recognized and named before a useful and meaningful classification can be constructed. The field of study relating to classification frequently is called “taxonomy,” although the broader term “systematics” is also widely used and is preferred by us. The goal of scientific nomenclature, one aspect of systematics, is to assure that each kind of organism has a unique name, and only one name. The Inter- national Code of Zoological Nomenclature (latest edition, Stoll, 1964) forms the accepted framework for dealing with nomenclature, both past and present. The presently reprinted paper by Glass and Baker points up one kind of nomenclatorial problem faced by the systematist (see also Bull. Zool. Nomen- clature, 22:339-340, 1966, and Glass and Baker, 1968, for further commentary on this same problem). The Code is administered by the International Com- mission on Zoological Nomenclature but, as Blair (1968) pointed out, the Commission “has no way of enforcing its decisions, and the burden of holding names to conformity with the [Code] falls on the individual worker and on editors of scientific publications.” Prior to the first decade or so of the 20th century, mammalian systematics generally was based on a “hit-or-miss” typological approach, which, although it fostered considerable advancement in cataloguing the faunas of the world, was limited in perspective and potential. The development of evolutionary thought and the spectacular growth of genetics have led to the “new syste- matics,” the biological species concept of today, as discussed in detail in such syntheses as Huxley (1943), Mayr et al. (1953), Simpson (1961), and Mayr (1963 and 1969), among others. Blackwelder’s (1967) and Ross’s (1974) texts on systematics also are deserving of mention here, as are treatises on special taxonomic methods such as Sneath and Sokal (1973) on phenetics and numer- ical taxonomy, and Hennig (1966) on cladistics. However, to infer that all early taxonomic treatments of mammals were either inconsequential or poorly conceived would be a gross error. Pallas’ (1778) revision of rodents, for example, was a monumental work far advanced for its day, as were many other outstanding contributions by 18th and 19th century mammalogists. Nevertheless, one has only to compare the descrip- tions and accounts of Pallas with those found in papers reprinted here by Merriam, Handley, and Genoways and Jones to appreciate the tremendous revolution in systematic practice. The short contribution by J. A. Allen not only provides an example of a review, but deals in some detail with two sub- stantial revisionary works published at the turn of the century. Among the larger modern revisionary studies that might be recommended to the student are those of Osgood (1909), Jackson (1928), Hooper (1952), Pearson (1958), Lidicker (1960), Packard (1960), Musser (1968), Choate (1970), Smith (1972), Birney (1973), and Genoways (1973); the last of these is especially noteworthy for its completeness in coverage of a mammalian genus. Eller- man’s (1940, 1941, 1948) well organized review of living rodents and Hill’s (1953 and subsequent volumes) somewhat more rambling and less critical coverage of the primates also are noteworthy attempts to summarize selected bodies of knowledge of important groups of mammals. Development of technologically advanced means of collecting, preparing, and storing specimens has resulted in the accumulation of series of individuals of the same species (the invention of the break-back mouse trap and Sherman live trap might be mentioned here along with the relatively recent widespread use of mist nets and specialized traps for capturing bats). This in turn allowed for assessment of variations within and between populations. Sophisticated studies of intergradation, hybridization, and speciation are examples resulting from technological and conceptual advances in this area, and have been greatly enhanced by development of multivariate statistics and computerized pro- grams for data analysis. The emphasis in this section is mostly at the level of species and subspecies (for example, the papers by Benson and by Lidicker). Higher categories are dealt with primarily in Section 5, although the contribution included here by Forman et al. deals with systematics at the familial level. Attempts over the years by systematists to standardize techniques and definitions are illustrated in the paper by Thomas. The short essay by Grinnell also bears on this point. Our final four selections illustrate the application of these techniques and concepts to specific systematic problems, all of which were clarified in ways that might have been impossible otherwise. Those by Genoways and Jones and by Forman et al. have been mentioned previously. The treatment by Bowers et al. of the problem of the relationship between two species of Peromyscus employs data from karyological and electrophoretic studies as well as breeding experiments. Genoways and Choate have used multivariate analy- sis to elucidate relationships among populations of the short-tailed shrew, in- cluding identification of hybrid individuals. Many papers in other sections of this anthology touch on systematics in one way or another, and the usefulness to the taxonomist of information from a variety of sources will be immediately evident to the reader. Two journals devoted to the concepts and practices of systematics and in which contributions to mammalogy regularly appear are SysreMATIC ZOOLOGY and ZEITSCHRIFT FUR ZOOLOGISCHE SYSTEMATIK. The Museum Conscience HE scientific museum, the kind of museum with which my re- marks here have chiefly to do, is a storehouse of facts, arranged acces- sibly and supported by the written records and labeled specimens to which they pertain. The purpose of a scien- tific museum is realized whenever some group of its contained facts is drawn upon for studies leading to publication. The investment of human energy in the formation and maintenance of a re- search museum is justified only in proportion to the amount of real knowledge which is derived from its materials and given to the world. All this may seem to be innocuous platitude—but it is genuine gospel, never-the-less, worth pondering from time to time by each and every museum administrator. It serves now as a background for my further comments. For worthy investigation based upon museum materials it is absolutely es- sential that such materials have been handled with careful regard for ac- curacy and order. To secure accuracy and order must, then, once the mere safe preservation of the collections of which he is in charge have been attended to, be the immediate aim of the curator. Order is the key both to the accessi- bility of materials and to the apprecia- tion of such facts and inferences as these materials afford. An arrange- ment according to some definite plan of grouping has to do with whole col- lections, with categories of specimens within each collection, with specimens within each general category, with the card indexes, and even with the place- ment of the data on the label attached to each specimen. Simplicity and clearness are fundamental to any scheme of arrangement adopted. Noth- ing can be more disheartening to a research student, except absolute chaos, than a complicated ‘‘system,” in the invidious sense of the word, carried out to the absurd limits rec’ amended by some so-called “efficiency expert.” However, error in this direction is rare compared with the opposite extreme, namely, little or no order at all. To secure a really practicable scheme of arrangement takes the best thought and much experimentation on the part of the keenest museum curator. Once he has selected or devised his scheme, his work is not done, moreover, until this scheme is in operation throughout all the materials in his charge. Any fact, specimen, or record left out of order is lost. It had, perhaps, better not exist, for it is taking space some- where; and space is the chief cost initially and currently in any museum. The second essential in the care of scientific materials is accuracy. Every item on the label of each specimen, every item of the general record in THE MusEuM CONSCIENCE the accession catalog, must be precise as to fact. Many errors in published literature, now practically impossible to ‘‘head off,’’ are traceable to mistakes on labels. Label-writing having to do with scientific materials is not a chore to be handed over casually to a ‘'25- cent-an-hour”’ girl, or even to the ordinary clerk. To do this essential work correctly requires an exceptional genius plus training. The important habit of reading every item back to copy is a thing that has to be acquired through diligent attention to this very point. By no means any person that happens to be around is capable of doing such work with reliable results. Now it happens that there is scarcely an institution in the country bearing the name museum, even though its main purpose be the quite distinct func- tion of exhibition and popular educa- tion, that does not lay more or less claim to housing ‘‘scientific collections.” Yet such a claim is false, unless an adequate effort has been expended both to label accurately and to arrange systematically all of the collections housed. Only when this has been done can the collections be called im truth scientific. My appeal is, then, to every museum director and to every curator responsi- ble for the proper use as well as the safe preservation of natural history specimens. Many species of vertebrate animals are disappearing; some are gone already. All that the investigator of the future will have, to indicate the 10 nature of such then extinct species, will be the remains of these species preserved more or less faithfully, along with the data accompanying them, in the museums of the country. I have definite grounds for present- ing this appeal at this time and in this place. My visits to the various larger museums have left me with the un- pleasant and very distinct conviction that a large portion of the vertebrate collections in this country, perhaps 90 per cent of them, are in far from satis- factory condition with respect to the matters here emphasized. It is ad- mittedly somewhat difficult for the older museums to modify systems of installation adopted at an early period. But this is no valid argument against necessary modification, which should begin at once with all the means avail- able—the need for which should, in- deed, be emphasized above the making of new collections or the undertaking of new expeditions. The older materials are immensely valuable historically, often irreplaceable. Scientific interests at large demand special attention to these materials. The urgent need, right now, in every museum, is for that special type of cura- tor who has ingrained within him the instinct to devise and put into opera- tion the best arrangement of his materials—who will be alert to see and to hunt out errors and instantly make corrections—who has the museum con- science. March 29, 1921. Vo. XVIII, PP. 191-196 SEPTEMBER 2, 1905 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON SUGGESTIONS FOR THE NOMENCLATURE OF THE CRANIAL LENGTH MEASUREMENTS AND OF THE CHEEK-TEETH OF MAMMALS. BY OLDFIELD THOMAS. Although various reasons prevent the general success of such a wholesale revolution in scientific terms as is described in Wilder and Gage’s Anatomical Technology (1882), where the many arguments in favor of accurate nomenclature are admira- bly put forth, yet in various corners of science improvements can be suggested which, if the workers are willing and in touch with each other, may be a real help in reducing the inconvenience of the loose or clumsy terminology commonly in vogue. Two such suggestions, due largely to the instigation of Mr. Gerrit 5. Miller, Jr., form the subject of the present paper. I. LenactH MEASUREMENTS OF THE SKULL AND PALATE. In giving the length measurement of the skull, not only do different authors at present use different measurements in de- scribing the skulls of similar or related animals, but in doing so they designate these measurements by terms of which it is often difficult or impossible to make out the exact meaning. Such a name as “ basal length’’ has I believe been used by one person or another for almost every one of the measurements to be here- 34—Proc. BIoL. Soc. WAsH., VoL. XVIII, 1905. 191 11 192 Thomas— Nomenclature of Measurements. after defined, and readers are expected to know by heart every- thing that the user has ever written on the subject, footnotes and all, in order to understand what is meant by the particular termemployed. Such a state of things has many inconveniences, and it is hoped the present communication, if it meets with the approval of other workers on the subject, may doa little toward putting an end to the existing confusion. As long ago as 1894,* by agreeing with Dr. Nehring for the definition of the terms basal and basilar in our own future writ- Cok akat fence ings, I made a first step in this direction, and the present is an amplification of the principle then adopted. All the difficulty has arisen from the fact that both at the anterior and the posterior ends of the skull there are two meas- urement points, so that there are four different ways in which the basal length of the skull may be taken, and under that name some authors have adopted nearly every one of them. It is clear that if a definite name be given to each one of the four measurements, authors, by using these names, will be en- abled to give the measurements they faney without causing con- fusion in the minds of their readers as to their exact meaning. *Ann. & Mag. Nat. Hist., Ser. 6, XIII, p. 203. 12 Thomas—Nomenclature of Measurements. 193 The different points are: Anteriorly: 1. THe GNaruion, the most anterior point of the premaxille, on or near the middle line. 2. THE HENSELION, the back of the alveolus of either of the median incisors, the point used and defined by Prof. Hensel in his cranio- logical work. Posteriorly: 3. THE Baston, a point in the middle line of the hinder edge of the basioecipital margin of the foramen magnum. 4. Tue Conpytion, the most posterior point of the articular surface of either condyle. A. fifth measuring point to be referred to below is the Pawa- TION, the most anterior point of the hinder edge of the bony palate, whether in the middle line or on either side of a median spine. Now using these words for.the purposes of definition, I would propose, as shown in the diagram, the following names for the four measurements that may be taken between the points above defined : — 1. BasaL LENGTH, the distance from Basion to Gnathion. 9. BASILAR LENGTH, the distance from Basion to Henselion. b 3. CONDYLO-BASAL LENGTH, the distance from Condylion to Gnathion. 4, CoNDYLO-BASILAR LENGTH, the distance from Condylon to Henselion. In addition there may be: 5. GREATEST LENGTH, to be taken not further divergent from the middle line than either condylion. A long diagonal to a projecting bulla or paroccipital process would thus be barred. If however the words ** between uprights ”’ be added the measurement would be between two ver- tical planes pressed respectively against the anterior and posterior ends of the skull at mght angles to its middle line. 6. Upper LenctTu, from tip of nasals to hinder edge of occipi- tal ridge in middle line. The difference between the words basal and basilar, which at first seemed trivial and indistinetive, is founded on the use of 13 194 Thomas— Nomenclature of Measurements. the English word basal by the older writers, such as Flower and others, who used the measurement from the gnathion; while basilar is an adaptation of the German of Hensel and his school, who used the “* basilar-lange’’ from the henselion. These hames again, combined with condylo-, readily express the points Which are used by those who like to adopt the condylion as a posterior measuring point. But further, the association of the ending ‘‘al’’ with a meas- ? with one from the henselion, if once defined and fixed, may be utilized in a second urement from the gnathion, and ‘‘ilar case of similar character. The length of the bony palate is a measurement given by all careful describers, but the anterior measuring point used is again either the gnathion or henselion, doubt as to which is being used often nullifying the value of the measurement altogether.* To avoid this doubt I would suggest, exactly as in the other case, that the name of the measurement from the gnathion should end in “‘al’’ and that from the henselion in ‘‘ ilar.’’ We should then have: PALATAL LENGTH, the distance from gnathion to palation. PALATILAR LENGTH, the distance from henselion to palation. The indeterminate “* palate length’? would then be dropped altogether. Il. THe NAMES OF THE CHEEK-TEETH OF MAMMALS. Although the cheek-teeth of mammals, the molars and _ pre- molars, have been studied and written about ever since the birth of zoology, no uniform system of naming them has been evolved and there is the greatest divergence between the usage of differ- ent workers on the subject. In old days all were called molars or grinders; then the premolars were distinguished from the true molars (although French zoologists, Winge in Denmark, and Ameghino in Argentina, continued to use a continuous notation for the two sets of teeth combined) and the usual habit among zoologists in general was to speak of them individually as “‘ second premolar,’’ ‘‘ third molar,’? and soon, Even here, however, an important difference cropped up owing to Hensel *T may explain that in my own descriptions the palate of any given animal has al- ways been measured from the same anterior point, gnathion or henselion, as the skull itself, this latter being indicated by the use of the words basal or basilar. 14 Thomas— Nomenclature of Measurements. 195 and his school in Germany numbering the premolars from be- hind forwards, while naturalists of other nations counted from before backwards, as with the incisors and molars, a difference often productive of fatal confusion. Of late years, however, partly owing to an increasing concensus of opinion that the seven cheek-teeth of Placentals, four pre- molars and three molars, are serially and individually homolo- gous with the seven of Marsupials, formerly reckoned as three premolars and four molars, many naturalists have again begun to think that a continuous numeration might be the best one. But the difficulties in the way of its adoption are very great, largely owing to the absence of any convenient and suitable word in English less clumsy than “* cheek-tooth,’’ to express a tooth of the combined premolar and molar series. To speak of the ‘* first cheek-tooth ’’ or of the ‘* predecessor to the fourth cheek- tooth’? would be so retrogressive a step that I am sure no one would adopt it. But if instead of trying to find a word for the series combined with a numeral to show the position, we were to have a name for each tooth, we should get some- thing of the immense convenience we have all realized in having definite names for the canine and the carnassial teeth, the latter name being found of value in spite of the fact that the upper and lower carnassials are not homologous with each other. Such hames might be made from the positions of the teeth if their meanings were not so obtrusive as to confuse the minds of per- sons who do not readily understand how a tooth should be called ‘the second ’”’ or ‘‘secundus’’ when it is actually the most an- terior of the series. Now it fortunately happens that while the Latin terms “‘ pri- mus,’’ “* secundus,’’ etc., express the serial positions too clearly for the convenience of weak minds, Latinized Greek terms have just about the right amount of unfamiliarity which would enable them to be used as names without their serial origin being too much insisted on. Moreover, their construction is similar to the process we all use in making generic names, and so far as I know they have never been previously utilized in zoology. Then, after Latinizing the Greek ordinal terms zpwrtes, ete. for the cheek-teeth of the upper jaw, the same modification as isalready used in cusp nomenclature might be adopted for those of the mandible. 15 196 Thomas— Nomenclature of Measurements. We should thus have, counting from before backwards: UPPER JAW. LOWER JAW. Cheek-tooth 1 Protus Protid " 2 Deuterus Deuterid ss 3 Tritus Tritid 4 Tetartus Tetartid a 5 Pemptus Pemptid ie 6 Hectus Hectid ‘i 7 Hebdomus Hebdomid To avoid any doubt, I would expressly allocate these names to the permanent teeth of placentals, leaving the names of the marsupial teeth to be settled in accordance with their placental homologies. For the milk teeth a further modification would be available by prefixing the syllable Pro- to the names of the respective permanent teeth. We could thus for example in the case of a third lower milk premolar call it the protritid, and so use one word instead of four. Of course I have no supposition that this system would ever be frequently or generally used, but I am convinced that in many special cases, and particularly in such descriptions and cata- logues of isolated teeth as paleontologists often have to give, it might result in considerable convenience and saving of space. 16 The Nature of Subspecies Boundaries ina Desert Rodent and its Implications for Subspecies Taxonomy T SEEMS to me that the wide diversity of opinion which exists concerning the usefulness of trinomial nomenclature re- volves in large measure on the more basic issue of whether or not it is possible to recognize infraspecific categories which reflect genetic relationships. As recently pointed out by Sneath (1961), taxonomic categories which are not based on rela- tionships are thereby rankless and cannot logically be included in a taxonomic hierarchy. Thus if the subspecies cate- gory is used merely as an instrument for describing geographic variation in a few characters or as a device for cataloging geographic variants (as is done by many taxonomists), artificial classifications of convenience are characteristically pro- duced. Such convenience classifications usually contain rankless groups (the “false taxa” of Sneath) which cannot be allocated in the taxonomic hierarchy. This is simply because categories based on a few arbitrary characters are themselves arbitrary, and lead to the objection of Brown and Wilson (1954) and others that trinomials based on one group of char- acters need not bear any relation to those based on different traits. Many of the same philosophical difficulties apply to systems such as that recently proposed by Edwards (1954) and Pimentel (1959) in which the subspecies would become a measure of isolation, by restricting its use to completely isolated and “obviously dif- ferent” populations. If on the other hand studies of infra- specific populations are focused on dis- covering evolutionary diversity or degrees of relationship between the various popu- lye WILLIAM Z. LIDICKER, JR. lations, I see no philosophical objection to the use of the trinomen. The question then reduces to one of the feasibility and/ or desirability of searching for such rela- tionships, and of deciding what level of dissimilarity if any justifies use of the formal trinomen. It is primarily these two subsidiary questions which are ex- amined in this paper, with the frank hope that the subspecies can be rescued from the rankless limbo of the morph, ecotype, and form. If this rescue operation should prove successful, attention can then be directed to other problems of greater bio- logical *nterest, such as whether or not determinations of genetic relationships within a species, which are based on phenotypes, can serve as a basis for specu- lations on phylogeny. Obviously geogra- phic relations would have to be con- sidered at this level, but, assuming that such information is taken into account, it would be highly informative to contrast phenetic and phylogenetic subspecies classifications. In any case, analyses of infraspecific relationships would very likely provide valuable clues concerning the environmental forces which have in- fluenced the development of the existing evolutionary diversity. In a previous paper (1960) I attempted to determine the genetic relationships among populations within a species of kangaroo rat (Dipodomys merriami Mearns, 1890) by a careful analysis of 20 morphological features. I concluded at that time that at least in well-known ter- restrial species an attempt to recognize relative relationships within a species was at least possible. And, at the same time it SUBSPECIES BOUNDARIES was apparent that (besides the philosophi- cal objections already pointed out) the subspecies category by itself was com- pletely inadequate for describing the complex geographic variation occurring in that species. It is the raw data from this former investigation that I have used here to test further the reliability of those tentative conclusions. The search for relationships among populations of the same species implies a search for total genetic differentiation (or at least its phenotypic manifestations), and hence of lineages with partially in- dependent evolutionary origins such that they have some internal homogeneity and their own adaptive tendencies. To detect this kind of differentiation it seems impor- tant to analyze, among other things, the populations occurring at the boundaries between differentiating groups, just as in the analysis of species relationships it is the boundaries between them, or areas of sympatry, where the most significant in- formation on relationships is to be found. This is not to say that information con- cerning the regions of greatest divergence or adaptive peaks (in this case peaklets) of infraspecific populations is not impor- tant, but only that such data should not be the only source material for taxonomic judgments. Thus it is the intent of this paper to focus attention on the previously all but ignored subspecies boundaries, and to examine the nature of these areas in Dipodomys merriami as I had pre- viously and without the benefit of this analysis defined them (Lidicker, 1960). Because the determination of these intra- specific units was guided in this case by a desire to find populations of comparable evolutionary relationship, careful scrutiny of the intergrading zones between them and surrounding areas should be of par- ticular interest. Comparisons will also be made with levels of differentiation in areas in which no subspecies boundary was recognized, as well as with one re- gion in which species level differentiation was postulated to have been reached by an island isolate. 18 161 The second and related purpose of the paper is to describe a method which helps to accomplish the first objective by meas- uring total differentiation, or lack of similarity, in many diverse characters, and hence is proposed as a criterion of relationship. But at the same time the technique does not require the hard working taxonomist to have either access to a digital computer or facility with matrix algebra. The Method Most quantitative techniques available to the systematist, which concern them- selves with determining relationships, and hence with similarities as well as dif- ferences, either involve the analysis of qualitative or discontinuous characters and thus are most useful at the species or genus level (e.g., Michener and Sokal, 1957; Lysenko and Sneath, 1959), or in- volve calculations sufficiently complex (e.g., Williams and Lance, 1958) that they are avoided by most practicing systema- tists. What seems to be needed is an ad- ditional technique which is sufficiently adaptable to handle continuously variable, as well as discontinuous, characters of diverse types (and so is useful in infra- specific studies), and which at the same time is sufficiently practical that it will be widely useful. To this end the following proposed method is dedicated. It is not intended as a substitute for discriminant function analysis (Fisher, 1936; Jolicoeur, 1959) and related methods which attempt to discriminate between previously con- ceptualized populations by using combina- tions of variables. An analysis of relationship should ideally compare relative similarities and not differences. However, since the num- ber of similarities between populations within a species is very large, it is much easier to measure their differences and consider that the reciprocal of the amount of difference represents a measure of similarity. Thus as the amount of differ- ence approaches zero, the reciprocal ap- 162 SYSTEMATIC ZOOLOGY proaches infinity. The problem then be- comes one of summing the amount of difference in many diverse characters. To do this we must be able to express the differentiation for each trait by a pure number (no units). Cain and Harrison (1958), for example, accomplished this by dividing the differences which they observed between means by the maxi- mum value recorded for each character. The resulting ratios, which they called “reduced values,’ express the observed differences in terms of a fraction of the maximum size of each character. Al- though this permits the comparison of diversity among traits of different abso- lute size, it does not take into account either the possibility that various char- acters may have different variabilities, or the statistical significance of the ob- served mean differences. Furthermore, maximum size would seem to be a statistic of dubious biological importance in con- tinuously varying characters. On the other hand, all of these important vari- ables, the variance of each trait, character magnitude, as well as a consideration of whether or not mean differences have a high probability of representing real dif- ferences, are taken into account by ex- pressing differentiation as a proportion between the observed differences between samples and the maximum amount of dif- ference expected on the basis of chance sampling variation. Only mean differ- ences greater than that amount which may be due to chance would then be con- sidered as real differences. For our pur- poses the maximum chance variation ex- pected in any comparison can be equated to the minimum difference required for statistical significance (at any given con- fidence level). This minimum significant difference (msd) can be calculated in a number of ways. One possibility is to (letermine the standard error of the mean for each character for each sample. Then in comparing two samples for this char- acter, 2 SE; +2SE; =msd. This provides a conservative estimate of msd with con- fidence limits usually well in excess of 19 95%. For large studies, however, these calculations would be extremely laborious, as well as perhaps overly conservative, and a short-cut is suggested. If we can assume that each quantitative character in a given species exhibits a characteristic variability throughout its range, then calculations would be tre- mendously reduced if we were able to de- termine the expected or pooled standard deviation (s,) and standard error (s,_) of samples for which say n3 20. Very small samples would have to be grouped with adjacent samples whenever possible, or if necessary either ignored or have Separate msd-values calculated for them. Under these conditions 4s)_represents our best estimate of msd. Unfortunately con- fidence limits cannot be calculated for its reliability, although again it is generally a conservative estimate. The statistic s, can be conveniently determined by averag- ing the weighted variances for several samples of adequate size (Hald, 1952: 395). Note that as the estimate of s, im- proves it approaches the population stand- ard deviation (¢), and hence is applicable to a wider range of sample sizes. Better estimates of s, require knowledge of the total number of individuals in each of the populations sampled (see Cochran, 1959: 72), an obvious impossibility in this type of problem. In the examples given in this paper 4s». was estimated by using the standard deviation of one large sample collected near the center of the species’ range, and by assuming n=20. This ex- pediency seemed justified because of the close similarity in values of s calculated for a given trait among several samples, and because of the likelihood that s ap- proaches ¢ under these circumstances. Still another method of deriving the statistic msd, but one not used in this re- port, involves a more laborious, but sta- tistically more precise, procedure. The confidence limits for the difference be- tween any pair of means can be calcu- lated (see Dixon and Massey, 1957:128) whether or not we assume that we know SUBSPECIES BOUNDARIES the variance characteristic of each trait (s?) or use only the pertinent sample variances (s? and s?). For a large study, the calculations are very much reduced if one can estimate s, (see above), and per- haps even use only samples in which n=20. If these simplifications are pos- sible, a pair of confidence limits can be computed which will be characteristic for each trait studied. In either case, one con- fidence limit gives us our msd, since mean differences greater than this can with a known probability be considered real. We need not be concerned with the possibility that the mean differences are even larger than those observed. Consider then only those characters in which the differences in the mean values (X,—x,) for a given pair of locations (samples) are greater than the minimum significant differences. Now, divide these significant differences in mean values by the minimum significant difference char- acteristic for that trait (or for that pair of samples). This procedure gives us our pure number which can be designated as Cpa aie d, for successive characters, each representing a measure of differen- tiation in one character between one pair of samples. Having defined the amount of differentiation in each character in terms of a pure number, we can now add these to arrive at an esti- mate of total differentiation in the char- acters studied (Sd,;). In interpreting this statistic in any real situation, however, it seems apparent that the distance between the two samples compared should be taken into account. Obviously an amount of total differentiation exhibited between two samples which are close together geo- graphically would be more significant than the same amount of differentiation between samples geographically distant. To compensate for this effect of distance, I have divided the total differentiation by the distance (in miles) between the two samples. The resulting figure, which I have called D or the Index of Differen- 20 163 tiation,! represents the proportion of sig- nificant change that occurs between the two locations per mile. Then the re- ciprocal of D easily gives us our measure of similarity between populations. D need now only be further divided by the total number of characters studied, including those of course in which no differentia- tion occurred, to arrive at the mean char- acter differentiation per mile (MCD/mi.). The importance of considering distance between samples will depend in large measure on the specific problem under in- vestigation. Obviously air-line distance between samples does not always accu- rately reflect the real magnitude of the distance or barriers between them. I feel that this is not a serious difficulty, how- ever, since we are concerned with the abruptness of differentiation between ad- jacent populations and not with barriers per se. Moreover, in some ways D acts as a measure of restriction on gene flow, be- cause, if distance is kept constant, D will tend to increase as gene flow is reduced. Another potential difficulty with the dis- tance calculation is that it carries the assumption that if the two localities be- ing compared were actually closer to- gether, the amount of total differentiation shown would be less. This is not always true because not only are there sometimes large areas which exhibit very little geo- graphic variation, but also there exist un- avoidable gaps in specimen collections. For these reasons I felt that in the pres- ent analysis of D. merriami it was neces- sary to consider both Sd; and D in assess- ing differentiation. One further complication seems worth considering. This concerns variation in the direction of change between different characters. It seemed to me more signifi- cant if one or two characters were found to change significantly in a direction op- posite to that of the other characters, than if they all changed in the same di- 1 Note that this is in no way similar to the “differentiation index” of Kurtén (1958) which compares growth gradients. 164 SYSTEMATIC ZOOLOGY rection. Thus for each such direction change, I arbitrarily added one half the d-value for that specific character to Xd. This also serves to oppose any tendency to give too much weight to characters which may not be entirely independent in their variation, or to those varying allo- metrically. Otherwise no allowance has been made for differentially weighting characters which might be considered to have greater phylogenetic importance. Presumably this could be readily done, if there were some sound basis for making such judgments. Sneath (1961), however, points out some of the dangers inherent in attempts to do this, and argues for considering each character equally. Table 1 summarizes the calculations for 3d, D, and MCD/mi. for one pair of localities in southeastern Arizona. Note that a value of 3.476 has been included in sd for color changes. Ordinarily color characters should be quantified so that they can easily be added into this scheme. Unfortunately in my study, I did not quantify in numerical terms the six color features analyzed. This necessitated my determining when significant changes had occurred by reference to the color descriptions of each sample. Whenever important color changes were found be- tween samples, I included in xd for each such change a figure which represented the average d-value for all pairs of locali- ties in the boundary region under study which exhibited the same number of color changes as the sample pair being calcu- lated. For example, if two samples dif- fered in three color features and if the average d for all pairs of samples in that region which also differed by three color features was 1.50, then 4.5 (3 x 1.50) would represent the combined value of d for the three color traits. Although this represents an unfortunate complication, it should not detract from the validity of the overall method being proposed. Figures 1, 2, and 3 show the differentia- tion observed in 20 characters in D. mer- riami in selected portions of its large range. It is important to emphasize that these 20 characters were chosen in the original investigation (Lidicker, 1960) independently of the conclusions of other authors concerning what they considered important characters in distinguishing subspecies. The list thus includes not only most of the “taxonomically impor- tant” characters of other authors but numerous additional features as well. I chose for illustration regions which dem- onstrate various levels of differentiation TABLE 1—CALCULATIONS FOR TOTAL DIFFERENTIATION, THE INDEX OF DIFFERENTIATION, AND THE MEAN CHARACTER DIFFERENTIATION PER MILE IN Dipodomys merriami For A PAIR OF LOCALITIES IN SOUTHEASTERN ARIZONA (VICINITIES OF THE HUACHUCA AND SANTA RITA Mountains 54 MILES APART). CHARACTER * X,-xX,(mm.) msd d, hind foot length 1.40 0.68 2.059 ear length 0.62 0.52 1.192 basal length of the skull 0.54 0.52 1.039 cranial length 0.78 0.48 1.625 rostral width 0.19 0.06 3.167 1 direction change (ear) (4d.) 0.596 2 color changes (2x. for those pairs of localities with two color changes) 3.476 =d; = 13.154 D= 0.244 MCD/mi. = 0.012 ** * See Lidicker (1960) for a description of these characters. : ** Total of 20 characters studied. 21 165 SUBSPECIES BOUNDARIES Bee > 40 020) >.35015)or »40« 20) >:25010)or>.35(<15) | >.20010)or ».25(K1C) > 15 (10) or.20(10) > 10 010) or >.15 (10) | [ses | >.0505) or ».10 (<10) [| <05 or ».05(<5) [J 20 Fic. 1. Observed differentiation of Dipodomys merriami in southeastern Arizona and adjacent Mexico and New Mexico. Numbers on the lines connecting the various sample localities represent the calculated values for D and in parenthesis Zd,. intensity of stippling is based on these same statistics. The scale associated with each map rep- resents a distance of 25 miles. See also the text for a more complete explanation of the figures. 22 The key to the 166 “Q2201360 O> So <6 Fallon * SYSTEMATIC ZOOLOGY 197 (979) 0) x, gala “a 3 ye vo Piz ny 9, aS > os mee ov Ovy 9) Nees oO = See fe) @ oOo 2 BB Ss S 9 orA/%®, © © io) > 902 [@) 2s. i oe oS Aguanga X Fic. 2. Observed differentiation of D. merriami in a) northern Nevada, b) southern Nevada and adjacent Mojave desert of California, and c) small area in extreme southern California. For a more complete explanation of the figures and a key to stippling intensity, see the text and Figure 1. ranging from essentially none to that judged to be at the species level. Figure 1 shows the boundary region between D. merriami merriami and D. m. olivaceus (nomenclature based on Lidicker, 1960) in southeastern Arizona and adjacent Mexico and New Mexico. Figure 2 illus- trates areaS in northern Nevada (a), southern Nevada and the adjacent eastern Mojave desert of California (b), and fi- nally a small area in southern California at the boundary of D. m. collinus and D. m. arenivagus (c). Figure 3 represents the southern tip of the Baja California peninsula (a), and southern Sonora where the boundary between D. m. mer- riami and D. m. mayensis is found (b). The first of these (3a) is of particular in- terest as it shows the entire range of D. m. melanurus and the adjacent island populations of D. m. margaritae and the presumed allopatric species D. insularis. Notice that the key takes into account both D and Sd (but gives greatest weight to D) and is arranged so that increased intensity of stippling represents increased differentiation. Heavy dashed lines repre- sent the locations of previously estab- lished subspecies boundaries, and double dashed lines previously established spe- cies boundaries (see Lidicker, 1960). Each drawing also indicates the location of one prominent town so that each chart can be placed geographically; all are ori- ented with north upward. SUBSPECIIS BOUNDARIES 167 ay b oO, 7 % O oO = Zs bs G5, oh oa sy) 1335 or) O On. SS %g_“O A5 Oo, Guaymas Fic. 3. Observed differentiation of D. merriami in a) southern Baja California, and b) southern Sonora. For a more complete explanation of the figures and a key to stippling intensity, see the text and Figure 1. Discussion of the Method The method described and its pictorial representation as shown in the figures gives us a geographically oriented sum- mary of statistically significant differen- tiation in the characters studied. Its most important feature is that it takes into ac- count the variability of each character as well as its magnitude, and concerns itself only with diversity which has a high probability of being real. Clearly, the more characters examined by the investi- gator, the greater will be his chance of 24 discovering all of the existing differences between populations, and the better will be his estimate of genetic diversity. In the present case there is a remarkable correlation between the subspecies and species boundaries as previously de- scribed by the author and the bands of rapid character changes as defined by the Index of Differentiation.? It is clear that in this case subspecies boundaries uni- 2 No particular correlation is evident, how- ever, with many of the taxonomic conclusions of previous authors. 168 SYSTEMATIC ZOOLOGY formly appear as relatively narrow zones of high levels of differentiation or low levels of similarity, and, although it can- not be determined from the figures, these are usually, but not always, in areas of partial or complete isolation between pop- ulations. If the Index method truly de- scribes genetic diversity, then our con- fidence is bolstered in the possibility of using the subspecies category for char- acterizing infraspecific lineages. Besides the degree of differentiation, other suggested criteria for the recogni- tion of such lineages include the following considerations: 1) the continuity of the zone of differentiation; 2) diversity of the two postulated adaptive peaks; 3) differ- ences in the environments to which the adjacent populations are adapted, or con- sideration of the possibility that the two populations are adapted to the same en- vironment in a different way; 4) geologic or paleontologic evidence of separate evo- lution. Moreover, it would seem to be a simple matter to devise modifications of the Index of Differentiation so as to in- corporate discontinuous and qualitative characters. This would extend the useful- ness of the method, not only to infraspe- cific populations which differ by such characters, but also to-the species level. However, above the infraspecific level the problems of convergence. giving different weight to different characters (that is identifying primitive or generalized char- acters), and correlated characters (see especially discussions by Cain and Harri- son, 1960) are aggravated. It might be added in passing, however, that these sources of error are not so great a prob- lem as might be expected, because the proposed method emphasizes large num- bers of characters and overall similarities. Under these circumstances a few con- vergent or pleiotropic traits would alter the results very little. Moreover, the problem of differentially weighting char- acters often leads into circular arguments as pointed out by Sneath (1961). Although the proposed method incor- porates a number of compromises with 25 mathematical sophistication, I think that it is sufficiently accurate to be of consid- erable utility to the practicing taxono- mist. Furthermore, several modifications are suggested for improving precision if this seems appropriate. The method will not of course make any decisions for the investigator, as it should not, but it will give him additional objective criteria on which to base his decisions. The fact that the conclusions suggested by the calcula- tions and analysis of D’s are similar if not identical to those proposed without the benefit of the method suggests that the method does not produce unreasonable results, and therefore must not suffer un- duly from its lack of statistical elegance. Discussion of Results An obvious, but important, conclusion derived from a study of the figures is that statistically significant differences can be found between the vast majority of the population pairs. This serves to empha- size what is really intuitively obvious, namely that the ability to prove that two populations are statistically different in one or several characters is only a meas- ure of the persistence and patience of the systematist. To base formal subspecific descriptions on this kind of evidence seems to me to be almost meaningless as well as a contribution to the degradation of the subspecies category to the extent of losing it as a legitimate member of the taxonomic hierarchy. Furthermore, this is precisely the philosophy which usually seems to nurture the widespread empha- sis on naming with its often accompany- ing neglect of relationships, which has stimulated so much critical comment (see for example Wilson and Brown, 1953, and Gosline, 1954). The description of differentiation pro- vided in the figures carries the further im- plication that all levels of differentiation are found in D. merriami, and no obvious dividing line between subspecies and non- subspecies, and species for that matter, is thereby indicated. The method thus gives SUBSPECIES BOUNDARIES ——_== us information regarding how different (or similar) populations are, but does not tell us which ones we should call subspe- cies. This finding is consistent with cur- rent concepts of intraspecific variation, and permits the systematist to decide what degree of relationship has phylo- genetic significance for the particular or- ganism involved, and finally what level, if any, he wants to recognize with formal subspecies descriptions. In the present example subspecific boundaries are found to be usually associated with continuous bands of differentiation characterized by D-values greater than 0.15. The fact that this study has failed to reveal some biologically meaningful divi- sion marking the subspecies level does not mean of course that some such divi- sion will not be possible in the future. However, such a line of demarcation is obviously not a prerequisite to the success of the proposed method, which only con- cerns recognition of degrees of evolution. Nevertheless, one possible criterion for such a division which occurs to me is the relationship between the observed gene flow between two adjacent populations and that amount expected on the basis of the extent of physical contact existing between them. If the observed gene flow turned out to be less than that expected, or discriminating in terms of what genes were allowed to flow, this would serve as an indication that partially independent lineages were involved. This idea would not diminish in any way the obvious im- portance of geographical barriers in in- hibiting gene flow, but merely suggests that some day it may be possible to ask the question—would a high level of differ- entiation persist between two geograph- ically partially isolated populations if the barrier were reduced or eliminated? Or to put it in another way, how much re- duction in the physical barrier between them can these two populations resist be- fore gene flow becomes free flowing? This genetic concept of a subspecies argues that there are numerous infraspecific pop- ulations which by virtue of their past iso- 169 lation (not necessarily complete) show some inhibition of gene flow between them and their neighbors, which would tend to slow down the dedifferentiation process. If the geographic isolation is current, the argument must be stated that such a reduction in gene flow would occur if they were not so isolated. This reason- ing is merely a corollary of the fact that not all attempts by a species for isolation and differentiation result in species for- mation. There are a number of reasons why gene flow might be inhibited in such cases, and one of these is interdeme ge- netic homeostasis (Lerner, 1954). Other factors might be partial ecological or be- havioral barriers to free interbreeding. Although this suggestion for a biologi- cally meaningful subspecies criterion is mainly speculative, it seems to me to be one possible direction that future develop- ments in intraspecific analysis might take. The following definition of a sub- species is thus perhaps premature, but is offered because it is only a slight modification of widely used current definitions, but yet incorporates the con- cept outlined above; at the same time it does not commit one to any specific cri- teria for the recognition of subspecies. A subspecies is a relatively homogeneous and genetically distinct portion of a spe- cies which represents a separately evolv- ing, or recently evolved, lineage with its own evolutionary tendencies, inhabits a definite geographical area, is usually at least partially isolated, and may intergrade gradually, although over a fairly narrow zone, with adjacent subspecies. This does not say that subspecies are “incipient spe- cies.” It does say that subspecies are populations which have made initial steps in the direction of species formation, such that they might form species if suitable isolating conditions should develop, or they may be populations which have not reached the species level and are dedif- ferentiating. Obviously most subspecies will not become species, and likewise the process of dedifferentiation may become relatively stabilized through diverse selec- 26 170 SYSTEMATIC ZOOLOGY Sa a eT tive pressures on either side of the inter- grade zone. It seems to me then that the Index of Differentiation or some similar device can give us an often needed additional cri- terion for judging relationship between populations. And it is these relative relationships that are of primary interest; and if used as guide lines to the recogni- tion of subspecies will permit the legiti- mate retention of this category in the taxonomic hierarchy. Such an evolution- ary philosophy applied to infraspecific analysis has a number of important ad- vantages, not least of which is that it focuses attention on the speciation proc- ess and not on geographic variation per se, and thus emphasizes that the steps which can lead to species divergence must be initiated long before the process is actually completed. Other advantages not already alluded to include a consistency in applying the concept of relationship to all taxa and hence justifying to some ex- tent the nomenclatorial equivalence of species and subspecies, provision of a more uniform goal for infraspecific sys- tematists, and greater usefulness of sub- species to non-taxonomists because of the greater nomenclatorial stability and more reliable predictability of genetic differ- ences in unstudied traits that would result. There is little doubt that this approach will be considered impractical in some groups of organisms, but this seems of relatively little importance to the present discussion. Whereas a technique must be usable, no limits should be placed on the conceptualization of direction and signifi- cance of inquiry. I have confidence that systematists are not so unimaginative that appropriate procedures will not rap- idly follow perception of important and necessary goals, as they have already done to some extent. Present day taxon- omy is fraught with practicality, but is nevertheless shaken by criticism as to where it is all leading. 27 Summary A growing dissatisfaction with much of what is now subspecies taxonomy and the associated indiscriminanit use of the trinomen has caused many taxonomists to re-examine the basic tenets of intraspe- cific analysis. This “soul searching” has raised the important questions of whether or not it is possible or even desirable to use the subspecies category as a rankable taxon below the species level in the taxo- nomic hierarchy and at what level of dis- similarity, if any, formal trinomial no- menclature becomes appropriate. It is argued here that if the subspecies is to be preserved from degradation to the level of the rankless morphs, ecotypes, and forms, it must be based on degrees of relation- ship or evolutionary divergence. More- over, the determinations of relative ge- netic relationships implies an emphasis on similarities between the various sub- populations comprising a species, as well as careful scrutiny of events occurring in the boundary regions between them. This paper is therefore concerned with characterizing some of these postulated boundary areas, as well as some areas of lesser and greater amounts of differentia- tion, in the kangaroo rat Dipodomys mer- riami, To accomplish this, a method is out- lined which serves to sum the observed statistically significant differentiation in many diverse characters between adja- cent populations. In doing this, the method takes into account the variability and magnitude of each character. The estimate of total differentiation thus ob- tained can then be divided by the distance between the samples being compared to give the Index of Differentiation (D). The reciprocal of this statistic can also be taken as a measure of similarity. The Index of Differentiation can be further divided by the number of characters studied to give the mean character dif- ferentiation per mile (MCD/mi.). The system involves no complicated mathe- matical procedures, and yet contains only SUBSPECIES BOUNDARIES minor compromises with statistical so- phistication. Furthermore it is readily adapted to visual portrayal and analysis. The results of this analysis demonstrate a very close agreement between levels of differentiation as determined by the In- dex of Differentiation and the taxonomic conclusions previously arrived at, when an attempt was made to base subspecies on the relative relationships among infra- specific populations. Under these condi- tions subspecies boundaries are uniformly characterized by a high level of differen- tiation which occurs over a relatively nar- row zone, and is usually but not always associated with partial or complete isola- tion between populations. Moreover the analysis has emphasized the nearly ubi- quitous occurrence of statistically signifi- cant differences between populations, and hence of the futility of basing formal sub- species on this kind of evidence. And finally a continuum of levels of differen- tiation was found, ranging from none at all to the species level. It is concluded from this evidence that it is indeed possible to gather evidence on the relative relationships of the vari- ous portions of a species, and it is sug- gested that data of this sort should form the foundation for subspecific diagnosis. This approach tends to focus attention on the speciation process itself instead of on geographic variation per se. Various other advantages of this system are pointed out, and speculation is presented concerning the possible determination of a biologi- cally meaningful division between sub- species and lesser categories. Acknowledgments I am greatly indebted to the following individuals who have critically read this manuscript, but who do not necessarily share the views which I have expressed: S. B. Benson, N. K. Johnson, O. P. Pear- son, F. J. Sonleitner, and C. S. Thaeler. The figures were prepared by G. M. Christman of the Museum of Vertebrate Zoology. 28 Lil REFERENCES Brown, W. L., Jr., and E. O. Wiuson. 1954. The case against the trinomen. System. Zool., 3:174-176. Cain, A. J.,.and G. A. Harrison. 1958. An anal- ysis of the taxonomist’s judgment of affin- ity. Proc. Zool. Soe. London, 131:85-98. 1960. Phyletic weighting. Proc. Zool. Soc. London, 135:1-31. CocHRAN, W. G. 1959. Sampling techniques. John Wiley, New York. Dixon, W. J., and F. J. Massey, Jr. 1957. In- troduction to statistical analysis. McGraw- Hill, New York. Epwarps, J. G. 1954. A new approach to infra- specific categories. System. Zool., 3:1-20. FISHER, R. A. 1936. The use of multiple meas- urements in taxonomic problems. Ann. Eu- genics, 7:179-188. GosLInE, W. A. 1954. Further thoughts on subspecies and trinomials. System. Zool., 3:92-94. HA.Lp, A. 1952. Statistical theory with engi- neering applications. John Wiley, New York. JoLicoEuR, P. 1959. Multivariate geographical variation in the wolf, Canis lupus L. Evolu- tion, 13:283-—299. KurTEN, B. 1958. A differentiation index, and a new measure of evolutionary rates. Evo- lution, 12:146-157. LERNER, I. M. 1954. Genetic homeostasis. Oliver and Boyd, London. LipIcKER, W. Z., Jr. 1960. An analysis of in- traspecific variation in the kangaroo rat Dipodomys merriami. Univ. .California Publs. Zool., 67:125-218. LYSENKO, O., and P. H. A. SNEATH. 1959. The use of models in bacterial classification. Jour. Gen. Microbiol., 20:284-290. Mearns, E. A. 1890. Description of supposed new species and subspecies of mammals, from Arizona. Bull. Amer. Mus. Natur. Hist., 2:277-307. MIcHENER, C. D., and R. R. Sokau. 1957. A quantitative approach to a problem in classi- fication. Evolution, 11:130-162. PIMENTEL, R. A. 1959. Mendelian infraspecific divergence levels and their analysis. Sys- tem. Zool., 8:139-159. SNEATH, P. H. A. 1961. Recent developments in theoretical and quantitative taxonomy. System. Zool., 10:118-139. WILLIAMS, W. T., and G. N. LANcE. 1958. Automatic subdivision of associated popu- lations. Nature, 182:1755. Witson, E. O., and W. L. Brown, Jr. 1953. The subspecies concept and its taxonomic application. System. Zool., 2:97-111. WILLIAM Z. LIDICKER, JR. is Assistant Curator of Mammals at the Museum of Verte- brate Zoology and Assistant Professor in the Department of Zoology at the University of California, Berkeley. 204 Bulletin of Zoological Nomenclature VESPERTILIO SUBULATUS SAY, 1823: PROPOSED SUPPRESSION UNDER THE PLENARY POWERS (MAMMALIA, CHIROPTERA). Z.NAS.) 1701 By Bryan P. Glass and Robert J. Baker (Department of Zoology, Oklahoma State University, Stillwater, Oklahoma, U.S.A.) 1. The purpose of this application is to request the International Com- mission on Zoological Nomenclature to use its plenary powers to suppress the specific name subulatus Say, 1823, as published in the combination Vespertilio subulatus (James’ account of Long’s Expedition from Pittsburgh to the Rocky Mountains, 2 : 65), and thus to ensure that the specific name Myotis yumanensis H. Allen, 1864 (Smithsonian Musc. Coll. 7 (Publ. 165) : 58) is conserved. 2. In 1823 Say collected a specimen of a species of Myotis near the 104th meridan on the Arkansas River, and described it in his notes, using the species name Vespertilio subulatus. His description was published verbatim as a footnote in James’ account of the expedition. Say did not state that the specimen was preserved; however, as far as is known, ail of his natural history collections were deposited in the Philadelphia Museum (Peale’s Museum) which was later destroyed by fire. Pertinent parts of Say’s description read as follows: **... flew rapidly in various directions, over the surface of the creek. ... Ears longer than broad, nearly as long as the head, hairy on the basal half, a little ventricose on the anterior edge, and extending near the eye: tragus elongated, subulate; the hair above blackish at base, tip dull cinereous; the interfemoral membrane hairy at base, the hairs unicolored, and a few also scattered over its surface, and along its edge, as well as that of the brachial membrane; hair beneath black, the tip yellowish white; hind feet rather long, a few setae extending over the nai!s; only a minute portion of the tail protrudes beyond the membrane. Total length 2 9-10 inches. tail 1 1-5.” 3. The description of Say fits M@. yumanensis, not M. subulatus (of Miller and G. M. Allen, USMN Bull. 144, 1928, and of later authors): M. yumanensis M. subulatus Dorsum dull cinereous Dorsum bright chestnut Uropatagium hairy at base Uropatagium naked at base Hind feet long Hind feet short Setae over nails No setae over nails Flies close to water Flies high 4. Myotis yumanensis is at present the only species of Myotis (other than the species currently referred to as subulatus) known from the vicinity of Say’s type locality, but the recognition of ywmanerisis in this region dates only from 1957. Other western Mvyoris possibly occurring in the vicinity may be excluded on the basis of one or more characters listed by Say: Myotis velifer—ears not hairy on basal half, hairs not blackish at base, size much too large; Myotis thysanodes—ears too long and not hairy on basal half, fringed interfemoral Bull. zool. Nomencl., Vol. 22, Part 3. August 1965. 29 Bulletin of Zoological Nomenclature 205 membrane, size much too large; Myotis volans—color brown, not dull cinereous, interfemoral membrane naked, size too large; Myotis lucifugus— color brown with burnished tips to hairs, not dull cinereous; Myotis cali- fornicus—color not dull cinereous, foot too small. 5. In 1855 Le Conte (Proc. Acad. Nat. Sci. Philad. : 435) applied the name Vespertilio subulatus Say to bats from his plantation in the tidewater country near Riceboro, Liberty County, Georgia. Miller and G. M. Allen (USNM Bull. 144 : 42, 1928) have indicated that Le Conte presumed that he had two species, to one of which he applied the name M. subulatus Say, but they pre- sumed that all the specimens were actually M. /ucifugus. Whatever the species actually was, it certainly was not the saxicolous species currently bearing the name M. subulatus, which is absent from the south eastern United States. 6. In 1864 Harrison Allen (Smith Miscl. Coll. No. 165 : 51) applied Say’s name to the eastern form of the long-eared bat, which usage was accepted until the revision of the genus by Miller and G. M. Allen (USNM Bull. 144, 1928) wherein they correctly rejected M. subulatus for the eastern long-eared Myotis in favor of the name M. keeni Merriam 1895, which is currently accepted, but erroneously applied the name Myotis subulatus Say to the form currently bearing the name. Miller and Allen (op. cit. p. 28) based this change, in part, on their imperfect knowledge of the bats known to occur in south eastern Colorado. 7. Identification of the species that Say had in hand when he wrote his description places in jeopardy the species name yumanensis which has stood unchallenged for 101 years. Such a change is not in keeping with the intent of the rules to promote stability. 8. The oldest species name available for the bat currently carrying the name M. subulatus Say is leibi published as Vespertilio leibii Audubon and Bachman, Jour. Acad. Nat. Sci. Philad. (1) 8 : 124, 1842. Suppression of the name subulatus requires that the subspecies of this taxon be as follows: Myotis leibi leibi Audubon and Bachman 1842, Type locality Erie County, Ohio. Myotis leibi ciliolabrum H. Allen, 1893, Type locality Near Banner, Trego County, Kansas. Myotis leibi melanorhinus Merriam 1890. Type locality Little Spring, North base of San Francisco Mountain, Coconino County, Arizona, Altitude 8,250 feet. 8. For the reasons listed above we now request the International Com- mission on Nomenclature: (1) to use its plenary powers to suppress the specific name subulatus Say, 1823, used originally in the combination Vesvertilio subulatus, for the purposes of the Law of Priority but not for those of the Law of Homonymy; (2) to place the name yumanensis H. Allen, i864, as published in the binomen Vespertilio yumanensis on the Official List of Specific Names in Zoology; and (3) to place the specific name subulatus Say, 1823, as published in the binomen Vespertilio subulatus, on the Official List of Rejected and Invalid Specific Names in Zoology. 30 REVIEWS OF RECENT LITERATURE. ZOOLOGY. Two Important Papers on North-American Mammals. — The literature relating to recent work on North-American mammals is so scattered, and the results have been the outcome of investigations by such a number of different workers, and based on such varying amounts of material, that it is a great gain when a competent author- ity on any given group can go over it and coordinate the efforts of his predecessors in the light of, practically, all of their material, combined with a vast amount in addition. In other words, the monographic revision of any of the larger genera of North-American mammals by an expert is a distinct advance, for which all mammalo- gists may well feel grateful. It is with pleasure, therefore, that we call attention to two recent contributions of this character — Mr. Vernon Bailey’s “ Revision of American Voles of the Genus Micro- tus,” and Mr. W. H. Osgood’s “ Revision of the Pocket Mice of the Genus Perognathus.” Mr. Bailey’s revision’ of the American voles, or meadow mice, is ‘‘based on a study of between five thousand and six thousand speci- mens from more than eight hundred localities, including types or topotypes of every recognized species with a known type locality, and also types or topotypes of most of the species placed in syn- onymy.” With such material at command, and with a wide experi- ence with the animals in life, and personal knowledge of the actual conditions of environment over a large part of the range of the group, Mr. Bailey has had peculiar advantages for his work, and his results are subject to revision only at points where material is still deficient, or from some other point of view. This revision, while obviously not final, presents a new starting point for future workers, and is likely to be a standard for many long years to come. The little animals here treated are the short-tailed field mice, 1 Revision of American Voles of the Genus Microtus. By Vernon Bailey, Chief Field Naturalist, Division of Biological Survey, U. S. Department of Agri- culture. Prepared under the direction of Dr. C. Hart Merriam, Chief of the Division. Morth American Fauna, No. 17, pp. 1-88, with 5 plates and 17 text- figures. Issued June 6, 1900. 221 31 222 THE AMERICAN NATORALIS T&S. [VOL. XXXV. familiarly typified by our common ‘meadow mice” of the Eastern States. The group is divisible into several well-marked subgenera, formerly generally known under the generic term ‘“ Arvicola,” which has had to give way to the less known but older term “ Microtus.” The group is especially distinctive of the northern hemisphere north of the tropics, and is found throughout North America from the mountains of Guatemala and southern Mexico northward, increasing numerically, both in species and individuals, from the south north- ward till it reaches its greatest abundance in the middle and colder temperate zones, again declining thence northward to the Arctic coast. They are vegetable feeders, and often do considerable dam- age to trees and crops ; they are active in the winter, forming long burrows or tunnels under the snow ; they are also very prolific, breed- ing several times a year, young being found throughout the warmer months. The seventy species and subspecies recognized by Mr. Bailey are arranged in nine subgenera; between the extreme forms the differ- ences are strongly marked, but the intermediate forms present grad- ual stages of intergradation. The subgenus Neofiber, of Florida, embracing the round-tailed muskrat, and the subgenus Lagurus, of the semi-arid districts of the northwestern United States, present the most striking contrast, not only in size but in many other features. The former is perhaps the largest known vole, while the latter group includes the smallest. Mr. Bailey’s paper, being a synopsis rather than a monograph, leaves much to be desired in point of detail, but is admirable in its way, and covers the ground with as much fullness as his prescribed limits would permit. Of the twenty-six synonyms cited, it is notice- able that thirteen relate to our common eastern meadow mouse, and date from the early authors, while two other eastern species furnish three others, also of early date. Only six of the remaining ten are of recent date, showing that of some fifty-five forms described within the last ten years, by nine different authors, forty-eight meet with Mr. Bailey’s approval. Four of the remaining seven are identified with earlier names which for many years have been considered indeterminable, but which Mr. Bailey claims to have established on the basis of topotypes. While he may be correct in these determinations, it would have been of interest to his fellow-specialists if he had stated the basis of his determination of certain type localities, notably those of Richard- son’s species, described as from the “‘ Rocky Mountains,” or similarly 32 NOAM KEL VILIV SSO? RECLNG TITERALURE, 993 vague localities. If he has some “ inside history ”’ to fall back upon, it is only fair that the secret should be made public. It may be said further, in the way of gentle criticism, that it is hardly fair wholly to ignore such knotty points as the allocation of a few names which he omits, since they form part of the literature of the subject, as, for example, Hypudeus ochrogaster Wagner, Arvi- cola noveboracensis Richardson, and some of Rafinesque’s names. Mr. Bailey describes as new two species and one subspecies. Mr. Osgood’s “ Revision of the Pocket Mice’’? is an equally wel- come contribution, and has been prepared upon much the same lines, with equal advantages in the way of material and field experience. The pocket mice of the genus Perognathus are confined to a limited portion of North America, being found only west of the Mississippi, and ranging from the southern border of British Columbia south to the valley of Mexico. They are strictly nocturnal and live in bur- rows, are partial to arid regions and seem to thrive even in the most barren deserts. ‘Their habits are hence not well known, as they are very shy and even difficult to trap. They are mouse-like in form, but only distantly related to the true rats and mice. Their most obvious character is the possession of cheek pouches which open externally. The pocket mice vary greatly in size, form, and in the nature of their pelage, which may be either soft or hispid ; but between the wide extremes there are so many closely connecting links that it is difficult to find any sharp lines of division, although two subgenera are fairly recognizable. The whole number of forms here recognized is 52 — 31 species and 21 additional subspecies, about equally divided between the subgenera Perognathus and Chetodipus. Of these, thirteen are here for the first time described. Out of a total of 61 specific and subspecific names applied to forms of this group, 9 are relegated to synonymy. Of these 61 names, it is interesting to note that 52 date from 188g or later, and that of these, eight prove to be synonyms, three of them having become so through the identi- fication of older names thought ten years ago to be indeterminable, but since reéstablished on the basis of topotypes. A previous revision of this group was made in 1889 by Dr. C. Hart Merriam, on the basis of less than two hundred specimens — 1 Revision of the Pocket Mice of the Genus Perognathus. By Wilfred H. Osgood, Assistant Biologist, Biological Survey, U.S. Department of Agriculture. Prepared under the direction of Dr. C. Hart Merriam, Chief of Division of Bio- logical Survey. North American Fauna, No. 18, pp. 1-72, Pls. I-IV, and 15 text- cuts. Issued Sept. 20, 1900. 33 994 THE AMERICAN NATURALIST. (Vou. XXXV. all of the material then available — when the number of currently recognized forms was raised from six to twenty-one. Dr. Merriam’s work, however, cleared the way for a better conception of the group, rectifying important errors of nomenclature and making known many new forms. Mr. Osgood, with fifteen times this amount of material, seems to have settled all of the remaining doubts regarding the appli- cation of certain early names, and, besides coordinating the work of his predecessors, has immensely extended our knowledge of the group. ‘The paper is admirable from every point of view and does great credit to its author. Aes No. 2, NORTH AMERICAN FAUNA, October, 1889, DESCRIPTIONS OF TWO NEW SPECIES AND ONE NEW SUBSPECIES OF GRASSHOPPER MOUSE, WITH A DIAGNOSIS OF THE GENUS ONYCHOMYS, AND A SYNOPSIS OF THE SPECIES AND SUBSPECIES. By C. Hart MeErRR1iaqM, M. D. A. DESCRIPTIONS OF NEW SPECIES AND SUBSPECIES. ONYCHOMYS LONGIPES sp. nov. (TEXAS GRASSHOPPER MOUSE.) Type 3335 9 ad. Merriam Collection. Concho County, Texas, March 11, 1887. Collected by William Lloyd. Measurements (taken in the flesh by collector).— Total length, 190™™ ; tail, 48 [this measurement seems to be too short]; hind foot, 25; ear from crown, 13 (measured from dry skin). General characters.—Size larger than that of the other known repre. sentatives of the genus, with larger and broader ears, and much longer hind feet. Earsless hairy than in O. leucogaster, with the lanuginous tuft at base less apparent; tail longer and more slender. Color.—Above, mouse gray, sparingly mixed with black-tipped hairs, and with a narrow fulvous stripe along each side between the gray of the back and white of the belly, extending from the fore-legs to the root of the tail; under parts white. Cranial characters.—Skull longer and-narrower than that of O. leuco- gaster (particularly the rostral portion), with much longer nasals, and a distinct supraorbital ‘+ bead” running the full length of the frontals and there terminating abruptly. The nasals overreach the nasal branch of the premaxillaries about as far as in leucogaster. The incisive foram. ina, as in OQ. leucogaster, barely reach the anterior cusp of the first molar. The roof of the palate extends further behind the last molar than in leucogaster, and gives off a median blunt spine projecting into the pterygoid fossa. The palatal bones end anteriorly exactly on a line 1 35 2 NORTH AMERICAN FAUNA. [No. 2. with the interspace between the first and second molars. The presphe- noid is excavated laterally to such a degree that the middle portion is reduced to a narrow bar less than one-third the width of its base. The condylar ramus is lower and more nearly horizontal than in leuwcogaster, and the angular notch is deeper. The coronoid process resembles that of lewcogaster. ONYCHOMYS LONGICAUDUS sp. nov. (LONG-TAILED GRASSHOPPER MOUSE.) Type 2334 g ad. St.George, Utah, January 4, 1889. Collected by Vernon Bailey. Measurements (taken in the flesh by the collector).—Total length, 145; tail, 55; hind foot, 20; ear from crown, 10 (measured from dry skin). General characters.—Similar to O. leucogaster, but smaller, with longer and slenderer tail. Pelage longer, but not so dense. General color above, ciunamon-fawn, well mixed with black-tipped hairs. Cranial characters.—Skull smaller and narrower than that of O. leuco- gaster; zygomatic arches less spreading; nasais less projecting behind nasal branch of premaxillaries. The coronoid and condylar processes of the mandible are shorter, and the coronoid notch is not so deep as in leucogaster. The presphenoid shows little or no lateral excavation. The incisive foramina do not quite reach the plane of the anterior cusp of the first molar. The shelf of the palate projects posteriorly consid- erably beyond the molars, and terminates in a nearly straight line with- out trace of a median spine. ONYCHOMYS LEUCOGASTER MELANOPHRYS subsp. nov. (BLACK-EYED GRASSHOPPER MOUSE.) Type, 243$¢ ad. Kanab, Utah, December 22, 1888. Collected by Vernon Bailey. Measurements (taken in the flesh by collector).—Total length, 154; tail, 41; hind foot, 21. Ear from crown 10 (measured from the dry skin). Size of O. leucogaster. Earalittlesmaller. Hind foot densely furred to base of toes. Color above, rich tawny cinnamon, well mixed with black-tipped hairs on the back, and brightest on the sides; a distinct black ring round the eye, broadest above. This ring is considerably broader and more conspicuous than the very narrow ring of leucogaster. Cranial characters.—Skull large and broad; very similar to O. leuco- gaster in size and proportions, but with zygomatic arches less spread- ing posteriorly, interparietal narrower, nasals not reaching quite so far beyond the nasal branch of premaxillaries, and antorbital slit narrower. Presphenoid moderately excavated, as in leucogaster. The incisive fo- ramina reach past the plane of the first cusp of the anterior molar. The condylar ramus is longer and directed more obliquely upward than in leucogaster, with the coronoid and infra-condylar notches deeper. NoTE.—In order to render the preceding diagnoses of new forms more useful, the following brief descriptions of the skulls of the two 36 OcT., 1889. | REVISION OF THE GENUS ONYCHOMYS. 3 revious ly known species are appended for comparison, together with figures of the skull of the type of the genus (0. leucogaster): Onychomys leucogaster Max.—Skull large and broad, with zygomatic arches spread- ing posteriorly. Antorbital slit larger than in the other known species. Palate hort, ending posteriorly in a short median spine (see figure). Onychomys torridus Coues.—Skull small , narrow, with zygomatic arches not spread- ing, and vault of cranium more rounded than in any other member of the genus. In- terparietal relatively large. Nasals projecting far beyond nasal branch of premaxil- lary. Incisive foramina very long, extending back to second cusp of first molar. Shelf of palate produced posteriorly nearly as far as in longicaudus, and truncated. Presphenoid slightly excavated laterally. Mandible much as in longicaudus, but with coronoid process more depressed and condylar ramus more slender. B. DIAGNOSIS OF THE GENUS ONYCHOMYS. The striking external differences which distinguish the Missouri Grasshopper Mouse from the other White-footed Mice of America (Hesperomys auct.) led its discoverer, Maximilian, to place it in the genus Hypudeus (=Evotomys, Coues), and led Baird to erect for its re- ception a separate section or subgenus, which he named Onychomys. Coues, the only recent monographer of the American Mice, treats Ony- chomys as a subgenus, and gives a Jengthy description of its characters. Since, however, some of the statements contained in this description are erroneous, and the conclusions absurd,* and since the most impor- tant taxonomic characters are overlooked, it becomes necessary to re- define the type. A somewhat critical study of the cranial and dental characters of Onychomys in comparison with the other North American White-footed Mice has compelled me to raise it to full generic rank. It may be known by the following diagnosis : Genus ONYCHOMYS Baird, 1857. Baird, Mammals of North America, 1857, p. 457 (subgenus). Type, Hypudeus leucogaster, Max. Wied, Reise in das innere Nord Amerika, 1, 1841, 99-101 (from Fort Clark, Dakota). Hesperomys auct. First and second upper molars large and broad; third less than half the size of the second. First upper molaft with two internal and three external cusps, the anterior cusp a trefoil when young, narrow, and on a line with the outside of the tooth, leaving a distinct step on the inside. Second upper molar with two internal and two external cusps, and a narrow antero-external fold. Last upper molar subcircular in outline, smaller than in Hesperomys, and less indented by the lateral notches. * Coues says: ‘‘ Although unmistakably a true Murine, as shown by the cranial and other fundamental characters, it nevertheless deviates much from Mus and Hesper- omys, and approaches the Arvicolines. Its affinities with Hvotomys are really close.” (Monographs of North American Rodentia, 1877, p. 106.) Asa matter of fact, Ony- chomys has no affinities whatever with Evotomys, or any other member of the Arvico- line series, its departure from Hesperomys being in a widely different direction. 37 4 NORTH AMERICAN FAUNA. [No. 2. Lower molar series much broader than in Hesperomys, First lower molar with an anterior, two internal, and two external cusps, and a postero-internal loop. In Hesperomys the anterior cusp is divided, so that there are three distinct cusps on each side. Second lower molar with two internal and two external cusps, an antero-external and a pos- tero-internal fold. Third lower molar scarcely longer than broad, sub- circular in outline, with the large posterior lobe of Hesperomys reduced to aslight fold of enamel, which disappears with wear. Coronoid process of mandible well developed, rising high above the condylar ramus and directed backward in the form of a large hook (see accompanying cut). Nasals wedge-shaped, terminating posteri- orly considerably behind the end of the nasal branch of the premaxil- laries. Vee \eE Fic. 1. Fie. 2. 1. Lower jaw of Onychomys leucogaster. 2. Lower jaw of Hesperomys leucopus. Body much stouter and heavier than in Hesperomys. Tail short, thick, and tapering to an obtuse point. Pore feet larger than in Hesperomys; five-tuberculate, as usual in the Murine series. Hind feet four-tuberculate, and densely furred from heel'to tubercles. Tubercles phalangeal, corresponding to the four an- terior tubercles of Hesperomys, that is to say, the first is situated at the base of the first digit, the second at the base of the second digit; the third over the bases of the third and fourth digits together, the fourth at the base of the fifth digit. The fifth and sixth (or metatarsal) tubercles of Hesperomys are altogether wanting. C. SYNOPSIS OF SPECIES AND SUBSPECIES. (1) By EXTERNAL CHARACTERS. Length, about 150™™; tail, about 40; hind foot, about 21; ear from crown, 10, Color above, mouse-gray; black ring around eye inconspicuous......-...0O. leucogaster. Size of O. leucogaster. Color above, rich tawny cinnamon, brightest on the sides; black ring round eye conspicuous...............------ O. leucogaster melanophrys. Length, about 145™™ ; tail, about55; hind foot, 20; ear from crown, 10. Color above, NTU YD STON OTP oh wy oe ep O. longicaudus. Length, about 190™™; tail, about 50; hind foot, 25; ear from crown, 13. Color above, mouse-gray, with a narrow fulvous stripe along the sides....-. O. longipes. Length, about 135™™; tail, about 45; hind foot, 20; ear from crown, 10. Color above, uniform dull tawny cinnamon; no black ring around the eye. Tail thick with a dark stripe above reachirg three-fourths its length; rest of tail white. O.~ torridus. 38 Ocr., 1889. ] REVISION OF THE GENUS ONYCHOMYS. (2) By CRANIAL CHARACTERS. with a blunt me- dian spine Palate ending posteriorly | with straight or | slightly con- | L vex edye 8 and nar- (skull large and broad a distinct supraorbital bead skull pee of first molar no distinct supraorbital bead..--- mr longipes. leucogaster. melanophrys. | jncisive foramina barely reach plane .---longicaudus. Cranial measurements of the known forms of the genus Onychomys. rower | incisive foramina reach second cusp of first molar torridus. | |Lon gipes, OG NeneOpest ets | Melanophrys, | Concho Dalotasn | Kanab, Utah. renee exas, 44182 441909 | 58935 | 58940 | 38399 Basilar length of Hensel (from furamen magnum to incisor).| 22 22 22.3 21.6 | 23.3 ZY comaticibresdth wees cease escaaesscemeceaee a= sen ae 15 15.2 15.4 15.5 15.5 Greatest parietal breadth .........--..--.---.-.ee ee eee eee 12.9 12.7 12.8 12.5 12.2 Interorbital:constriction =... 22222555 ssieseaneccinceis ase wan 4.5 4.5 §.2 4.8 4.4 Length of nasals.............-.... SEA RARE HO nCObU apoUscanr 10.8 11.6 10.7 10.7 12.5 Incisor to post-palatal notch...........-..--------2--+---. 12 1] 17 11.5 12.4 Foramen magnum to incisive foramina .....-...-..--..-- 14.7 14.6; 15 14.5 15.7 Foramen magnum to palate .. ....-...2....2.2 eee sees ee 9.7 10 10.2 9.9 10.6 Length of upper molar series (on alveol@) .-.-.-...---.-- 4.5 4,2 4.6 4.8 4.4 Length of incisive foramina. ...............----2--02--0ee- 5 5.7 5 5 5.3 Wength ofmandible!<-..-220-a2o- sen cones ~csoine Jo sece eae 5eo 15.8 1527 15.3 16 Height of coronoid process from angle ....-.....----- ache 6.5 (ee 6.8 6.8 7.2 Ratios to basilar length: Ay POmMatiowbreadGh oc. a2. o sc siesieciceies esisiessiscis sissies = 68.1 69 69 lind 66.6 Parietal preadthives sce ccce acer sco ccine/ lacie semiicicieisoe 58.9 57.7 57.3 57 52 Nasal 22 cece ccs cece esisioie cc seicre nieisiale d's cinia'clejate cisrerciseicts 49 52.7 47.9 49.5 52.3 Molar series (on alveol@) ................--2--------- 20.4 1y 20.6 22 20 UNCiSive FOLAMING 2 esos ne aa] aoa] | ad _— i) acd ae ee oO = a ee =. ot ae by) wo i) 5 Oo = = ~ 3 n =] rs) a ty 2 CD) cose BS 5 a a 2 = (op tae) re qo ic) = 10 i=) ~o | nl oe | op) al a S onan) pal al Ze) 4 fo) ond a (ae) bo wD o r= [| a 3 ol So 1 oD iol fo! A 3 oe o al Za 60 = Lone (2) os | t bh + oo Leal o OY 00 ol ao 1 ea) Ll a) 40S alt od r=t Ls Ol oo | = 24 19 Ato ONAN aioe! eee eel ier cot lee oe =) Ar Oo = =e -) cy19 Ol Hin ane aAaANo oe I | Le Bl os | al cal Coise. iS ato mow tc I | tes | Ne) wera as oto ow + Se Se xo} o ~ op) non BF ac ato + oor 44 D ae = a o aa wn m0 rH ac lease} ome eee) ae fom hh | wn 1 02 01 ao Ato ~~ on ae ae op) NAA 9 ano CO =H 4 ae oe = oe SS ano ~~ xt CD =e ee ie.) aon ne ato ow Crm ic | ae se) OD Ss ow ano rw =e =e ee € so =} ce ¢ aes S.5 x 36'S EG ®.6 ZAAa 22a S 19 mo all Od S ° S els O20 a ACA Lome ml o Ne) © reo S ancrod ee Lon co a ce eee S Oor~ce ool i) ° 1D winin S a aAaavood oe rc) Se DOA S) aoOorsd Lal et oo) Yel i CO Om ° DOrGAS al lo So onordn S = ; 5 ® : Z oo ° Ors) ee SO : So BPAXGBHSS Larods 3 3 3) = a a o a oa 2 COND OO So DABHS i>) — al anoa 4 raonrad op) Su 19 ain So a i ole ofce) — ml ° a ot SoC e Kea tHOoOrad Lomi | be a SQ CUS UES Ko COr ads Lom 1D — ae SS sen Ko rLADAS ee Ll = ce € re ze 5 36:5530.4 864 3653) 36.2) 35.8) So.0 B4e1 Interorbital constriction Sample 10 2) 8 2 5 6 4 i bf o tired as. 14 Mean 14 140 14.0) 165 W354 1s45 13.2 32 ise ls tose SON 12.6) Az Color (red reflectance ) Sample 7 14 #1 6 5 9 i Deemeel2, 8 3 A lS ae Mean US 2S OMS: 17-2 V1698 16.37 Vo:69 15-5) 1b AS Wb 2 a6 14 ae aes a 3 and 4, which are from relatively high elevations as compared with other samples from Jalisco and Zacatecas. Specimens from Tlaxcala (11) also had high values of reflected red. The two samples (12 and 13) that often grouped with sample 11 in external and cranial measurements fell among those with the low mean values for red reflectance. The sample from the vicinity of Mexico City (sample 10) had the lowest mean reading for red reflectance. The average value for this sample is a full 2 per cent less in reflectance than is the next lowest mean value (sample 13). Samples fell into three broadly overlapping, nonsignificant subsets for reflectance of green and four for reflectance of blue. They revealed approxi- mately the same relationship as for reflected red. Sample 10 had a much lower mean than the other samples for green and blue, as it did for red. Multivariate Analysis Means for each sample for the three external and six cranial measurements and three color reflectance values were used in a NTSYS-multivariate analysis. Phenograms diagramming the phenetic relationships of southern banner-tailed kangaroo rats were computed by cluster analysis from both distance and cor- 61 May 1971 GENOWAYS AND JONES—SYSTEMATICS OF DIPODOMYS 275 ee | FSS ences | ee eueeeneeeneaeses | eee eee a 2.24 1.84 1.44 1.04 0.64 0.24 Fic. 1—Distance phenogram resulting from cluster analysis of 15 geographic samples (see Fig. 2) of southern banner-tailed kangaroo rats. relation matrices; the phenogram based upon the distance matrix is pre- sented in Fig. 1. The samples in this phenogram are divided into two major clusters, one consisting of samples 14 and 15 and the second containing all others. Samples 14 and 15 are distantly separated in the first cluster. In the second cluster there are at least four major subclusters. Two of these consist of single samples 9 and 10, but the other two contain five (3, 4, 8, 12, and 13) and six samples (1, 2, 5, 6, 7, and 11). The coefficient of cophenetic correlation for the distance phenogram was 0.931. Fig. 2 indicates the approximate areas from which the samples were drawn and the distance coefficient between the connected samples. In most cases, for ease of diagrammatic presentation, we have connected only adjacent samples. The largest distance coefficients were found between samples 13 and 14 (2.568) and between 13 and 15 (1.815). Distance coefficients of more than 62 276 JOURNAL OF MAMMALOGY Vol. 52, No. 2 108 102 26 i L r ! Gye! hI < Y Ii ‘ +f \ ¢ : { \ we, = \ ~ we A ( \d + 0 ¢ 24h 0 “ts : Soy! \ oe \ 24 { \ 3 ee Ba 418 | 0, 100 200 400 Miles Paes 7 ut 9 100 | 300 500. Kilometers aa gla a Hie ! (te 108 102 96 Fic. 2.—Map showing geographic location of 15 samples of southern banner-tailed kangaroo rats used for numerical analysis in this study, and distance coefficients between adjacent samples. 1.00 were generated between samples 9 and 10, 10 and 11, 10 and 13, and 14 and 15, and a coefficient of 0.971 was found between samples 11 and 13. Distance coefficients of 0.8 to 0.9 were common, being found between six sets of localities. The first three principal components were computed from the matrix of correlation among the 12 characters. The first principal component expresses 64.16 per cent of the phenetic variation, the second 19.09, and the third 6.30. Two-dimensional plots of the three principal components are shown in Fig. 3. From the results of the factor analysis (Table 5), it appears that both external and cranial size had a strong influence on the first component. With respect to positioning of samples along component I, the sample containing specimens that were smallest overall (14) is located on the far right; from that point, samples are arranged in ascending order relative to size, with the sample consisting of the largest individuals (sample 9) on the far left of the plot. Major factors in the second component were the color reflectance ratings, although depth of cranium and mastoid breadth had some influence. The positioning of samples along component II reveals that sample 10, which contained the darkest individuals, is near the top of the plot, and that samples 3 and 4, which also had low reflectance readings, occupy a somewhat lower May 1971 GENOWAYS AND JONES—SYSTEMATICS OF DIPODOMYS bo ~] x] Fic. 3.—Two-dimensional projections of the first three principal components, illustrating the phenetic position of 15 samples of southern banner-tailed kangaroo rats. Top, com- ponent I plotted against component II; bottom, component I plotted against component III. 64 278 JOURNAL OF MAMMALOGY Vol. 52, No. 2 TABLE 5.—Factor matrix from correlation among the 12 characters studied. Factor Factor Factor Measurement Component I Component II Component III Total length —0.922 0135 0.150 Length of tail —0.867 —0.159 -0.043 Length of hind foot —0.947 —0.072 —0.077 Greatest length of skull —0.848 —0.163 0.423 Length of maxillary toothrow —0.891 —0.109 —0,224 Depth of cranium —0.867 —0.246 0.195 Mastoid breadth —0.854 —0.230 0.330 Maxillary breadth -0.891 =O137 —0.277 Interorbital constriction —0.805 —0.093 —0.505 Reflected red 0.332 —0.904 —0.106 Reflected green 0.467 —0.852 —0.050 Reflected blue 0.659 =(0:720 0.065 position on the component. Near the bottom of component II are samples that averaged high in reflectance readings. Factor analysis (Table 5) indicates that loading in the third component had high positive values for greatest length of skull and mastoid breadth and high negative values for maxillary breadth and interorbital constriction. The three samples (11, 12, and 13) that separate from the others in the third principal component are those that were shown in the univariate analysis to have among the largest means for mastoid breadth and among the smallest for maxillary breadth and _ inter- orbital constriction. The single specimen in sample 15 also appears to fall in the third component with samples 11, 12, and 13, but it is widely separated from these samples in component I, which indicates that in overall size this specimen is much smaller than those in samples 11, 12, and 13. Bacular Morphology The bacula of Dipodomys ornatus (Lidicker, 1960b:496) and Dipodomys phillipsii (Burt, 1960:45) have been figured previously, but no comparison between them has been made. Burt (op. cit.) stated that the morphology of the single baculum from a Oaxacan specimen that he examined differed from all others in the genus in that the tip is upturned at a sharp angle from the shaft. This is not the case, however, in bacula of two specimens that we examined from México and Veracruz. These do have an upturned tip (Fig. 4), but the angle between the tip and shaft appears similar to that figured by Burt (1960:pl. 12) for other Dipodomys. The bacula of four specimens from within the previously understood range of ornatus (two from Jalisco, one each from Zacatecas and Guanajuato) agree morphologically with those figured by Lidicker (1960b:496) from Aguascalientes. Little difference is evident in construction and morphology of the bacula of ornatus and phillipsii. That of ornatus is somewhat the larger, but it should be noted that the bacula of phillipsii we examined were from young adults, 65 May 1971 GENOWAYS AND JONES—SYSTEMATICS OF DIPODOMYS 279 C 1mm Fic. 4—Bacula of four southern banner-tailed kangaroo rats. Specimens represented (from top to bottom) are as follows: KU 19384, 2 km E Perote, Veracruz; KU 48987, 5 mi. S, 1 mi. W Texcoco, México; KU 48975, 8 mi. SE Zacatecas, Zacatecas; KU 48986, 4 mi. N, 5 mi. W Leon, Guanajuato. because no other material was available. Bacular measurements are as follows (specimens from, respectively, México, Veracruz, Burt’s rat from Oaxaca, Zacatecas, two from Jalisco, Guanajuato, mean and range of five bacula from Aguascalientes examined by Lidicker): length of baculum, 10.0, 9.1, 10.5, 11.3, 113, JE, ths; 12.2 (17-12.7 )s. height-of ‘base, 1:3, 1.4, 1.3). 1.6, -2.0:..2:0; 1.4, 1.8 (142.2); width of base, 1.0, 0.9, 1.2, 1.6, 1.5, 1.6, 1.8, 1.6 (1.5-1.9). Taxonomic Conclusions We interpret the univariate and multivariate analyses as revealing that southern banner-tailed kangaroo rats represent one geographically variable species. The relatively minor cranial variations that Merriam (1894:110-111) used to characterize D. ornatus (such as a flatter cranium) are the result of individual and geographic variation within a population of this species. Therefore, in the following accounts all southern banner-tailed kangaroo rats are treated as a single species, Dipodomys phillipsii Gray. 280 JOURNAL OF MAMMALOGY Vol. 52, No. 2 Within D. phillipsii, we recognize four subspecies. In the north, from Querétaro to central Durango, is Dipodomys phillipsii ornatus, which is char- acterized by medium to large size, relatively pale coloration, and medium to broad cranium. The nominate race, Dipodomys phillipsii phillipsii, is confined to the Valle de México and immediate vicinity; it is characterized by medium size, dark coloration, and broad interorbital region. Dipodomys phillipsii perotensis, which occurs in Tlaxcala, Puebla, and Veracruz, can be distinguished by large size, coloration intermediate between that of ornatus and phillipsii, a broad mastoid region, and narrow interorbital and maxillary regions. The fourth subspecies, Dipodomys phillipsii oaxacae, known trom northern Oaxaca and southern Puebla, is much smaller than the others and pale in color. SYNOPSIS OF SUBSPECIES The four recognized subspecies of D. phillipsii are briefly described in the following accounts, and pertinent commentary is included on distribution and infrasubspecific variation. In the lists of specimens examined, localities in italic type are not plotted on the accompanying distribution map (Fig. 5) because crowded symbols would have resulted. Dipodomys phillipsii phillipsii Gray 1841. Dipodomys phillipii [sic] Gray, Ann. Mag. Nat. Hist., ser. 1, 7:522 (see Coues, 1875:325, and Coues and Allen, 1877:540, for emendation of spelling). Type locality—‘‘near Real del Monte,” Hidalgo. Distribution Confined to Valle de México and immediately adjacent areas in Hidalgo, México, and the Distrito Federal (see Fig. 5). Remarks.—The nominal subspecies is characterized by dark dorsal coloration, broad maxillary and interorbital regions relative to mastoid breadth, and in being medium for the species in general size. For comparison of D. p. phillipsii with other subspecies of the species, see accounts of those taxa. According to Merriam (1893:84-86), after collecting a large series of D. phillipsii near Mexico City, E. W. Nelson attempted to obtain specimens in the vicinity of the type locality, Real del Monte, Hidalgo, at the extreme northern edge of the Valley of Mexico. His search in the vicinities of Real del Monte, Pachuca, Tula, San Agustin, and Irolo, all in Hidalgo, proved unsuccessful, although en route from Pachuca to Irolo, Nelson noted an area south of Pachuca that he believed might be suitable habitat for these kangaroo rats. Based on his failure to obtain specimens near the type locality, Nelson concluded that the locality recorded by Gray was erroneous and that the holotype most likely had originated from somewhere near Tlalpam, which was one of the important cities in the Valley of Mexico in the mid-1800’s, and a place where D. phillipsii was abundant. Later, however, a specimen was obtained on 22 August 1942 (Davis, 1944:391) at a place 85 km N Mexico City (approximately 9 km S Pachuca, Hidalgo) casting considerable doubt on Nelson’s conclusion. We believe it best to consider that the holotype of Dipodomys phillipsii came from the vicinity of Real del Monte, Hidalgo, at least until more convincing evidence to the contrary is available. The one specimen examined from south of Pachuca (TCWC 3028) is a male with deciduous premolars and still in juvenile pelage. The pelage of this specimen is darker than in juveniles of ornatus, but paler than in juveniles of typical phillipsii. The possibility exists that specimens from this area represent intergrades between ornatus and_ phillipsii, but 67 May 1971 GENOWAYS AND JONES—SYSTEMATICS OF DIPODOMYS 281 108 102 96 T T T pr Af 24- Ns iD 424 a f ISt \ ie ae a a Dan aie) oe ae zs hs Se SS (e) 100 200 400 Miles ‘ SS 4 4 1 J ae Oo 100 300 500 Kilometers a 27 SS ee ee ae | ! 108 102 96 Fic. 5.—Distribution of subspecies of Dipodomys phillipsii: 1, D. p. phillipsii; 2, D. p. ornatus; 3, D. p. perotensis; 4, D. p. oaxacae. adults are needed before any definitive statement can be made. One of us (Jones) did, however, examine the holotype (a badly preserved skin unaccompanied by skull) in the British Museum; its dorsal coloration is relatively dark, more or less typical of that found in specimens herein assigned to phillipsii. Merriam (1893:86), quoting Nelson’s field notes, stated that “they [D. phillipsii] were noted close to the peak of Huitzilac, near the Cruz del Marquez, at an altitude of 9000 feet.” We have not seen specimens from this locality and it is not clear whether Nelson collected the rats there. Specimens examined (38).—HIDALGO: near Real del Monte, 1 (BM—the holotype); 85 km N Mexico City, 8200 ft, 1 (TCWC). MEXICO: 5 mi. S, 1 mi. W Texcoco, 7350 ft, 1 (KU); 2 km S Huatongo, 2700 m, 1 (UNAM); Amecameca, 3 (USNM). DISTRITO FEDERAL: 17 km ESE Mexico City, 1 (TCWC) [labeled as in México, but reported as in the Distrito Federal by Villa-R., 1953:404, and Alvarez, 1961:409]; Cerro de la Caldera, 2300 m, 1 (ENCB); Tlalpam, 26 (USNM); km 20 de la cerretera México-Tldhuac, 1 (UNAM); Ajusco, 2 (USNM). Dipodomys phillipsii ornatus Merriam 1894. Dipodomys ornatus Merriam, Proc. Biol. Soc. Washington, 9:110, 21 June. Type locality—Berriozabal, Zacatecas. Distribution.—Recorded from the Mexican states of Durango, Zacatecas, Jalisco, Aguascalientes, San Luis Potosi, Guanajuato, and Querétaro. The northernmost record of occurrence is in the vicinity of Santa Cruz, Durango, and the southernmost is at Tequis- quiapam, Querétaro (see Fig. 5). Remarks.—This subspecies occupies the northern segment of the geographic range of the southern banner-tailed kangaroo rat. It is characterized by medium to large size and 68 282 JOURNAL OF MAMMALOGY Vol. 52:-No. 2 pale coloration. D. p. ornatus can be distinguished from D. p. phillipsii by its much paler color and relatively narrow interorbital region (57.9 to 60.9 per cent of mastoid breadth in nine samples of ornatus as compared with an average of 62.7 per cent in phillipsii). From D. p. perotensis, the subspecies ornatus differs in having a somewhat shorter skull on the average (greatest length in nine samples of ornatus ranged from 35.5 to 37.2 and in three of perotensis from 37.3 to 37.5), relatively broad maxillary and interorbital regions (maxillary breadth 94.2 to 96.6 per cent of mastoid breadth in ornatus and 89.3 to 90.8 in perotensis, interorbital breadth 57.9 to 60.9 per cent of mastoid breadth in ornatus and 54.8 to 57.2 in perotensis), and somewhat paler color. D. p. ornatus is easily distinguished from D. p. oaxacae by its much larger size. A general increase in size in several cranial measurements was noted from north to south within the geographic range of ornatus. Samples from Durango generally had the smallest mean values, whereas those from Zacatecas, Aguascalientes, Jalisco, and San Luis Potosi were intermediate in size, and samples from Guanajuato and Querétaro had the largest mean values. Specimens from relatively high elevations (especially samples 3 and 4) average slightly darker in color than do those from lower areas. Baker (1960:315-316) reported that individuals from the Guadiana lava fields (sample 2) were somewhat darker than typical specimens of ornatus. We find they are darker than rats from the vicinity of the type locality (sample 5), but that they are only slightly darker (revealed only in reflected green) than other specimens from Durango (sample 1), and that specimens from samples 3 and 4 are darker than those from the lava field in all three color readings taken (see Table 3). Specimens from Tequisquiapam, Querétaro (9), show some tendencies toward D. p. phillipsii, but clearly are assignable to ornatus. They have the broadest interorbital region relative to mastoid breadth (60.9 per cent) of any sample of ornatus, and are somewhat darker than adjacent populations (as seen in reflectance readings of green and blue). Nevertheless, in all of these characters, the specimens from Querétaro resemble ornatus to a greater degree than phillipsii. Alvarez (1961:409) cited from Dugés a record of Dipodomys phillipsii from San Diego de la Unién, Guanajuato. This record is of interest because it fills an otherwise rather broad gap in the known distribution of the species. Specimens examined (141).—DURANGO: SE end Laguna de Santiaguillo, Santa Cruz, 4 (KU); 9 mi. N Durango, 6200 ft, 1 (KU); 6 mi. NW La Pila, 6150 ft, 10 (MSU); 4 mi. S Morcillo, 6450 ft, 1 (MSU); Durango, 4 (USNM); 16 mi. S, 20 mi. W Vicente Guerrero, 6675 ft, 6 (MSU). ZACATECAS: 12 mi. N, 7 mi. E Fresnillo, 4 (UNM); Laguna Valderama, 40 mi. W Fresnillo, 7800 ft, 6 (CAS); Valparaiso, 16 (USNM); Zacatecas, 4 (USNM); 2 mi. S, 5 mi. E Zacatecas, 7700 ft, 1 (MSU); 8 mi. SE Zacatecas, 7225 ft, 4 (KU); 2 mi. ESE Trancoso, 7000 ft, 1 (KU); Hda. San Juan Capistrano, 3 (USNM); Berriozabal, 2 (USNM); 2 mi. N Villanueva, 6500 ft, 1 (KU); Plateado, 5 (USNM). SAN LUIS POTOSI: 1 km N Arenal, 1 (LSU); 1 mi. W. Bledos, 1 (LSU); Bledos, 1 (LSU). JALISCO: La Mesa Maria de Leén, 7400 ft, 14 (KU); 10 mi. NW Matanzas, 7550 ft, 5 (KU); 1 mi. NE Villa Hidalgo, 6550 ft, 5 (KU); 5% mi. N, 2 mi. W Guadalupe de Victoria, 7700 ft, 1 (MSU); 8 mi. W Encarnacion de Diaz, 6000 ft, 2 (KU); 2 mi. SW Matanzas, 7550 ft, 13 (KU); Lagos, 1 (USNM). AGUASCALIENTES: 7 mi. N Rincén de Romos, 1 (UNAM); 5 mi. NNE Rincén de Romos, 2 (KU); 3 mi. SW Aguascalientes, 6100 ft, 1 (KU). GUANAJUATO: 4 mi. N, 5 mi. W Leon, 7000 ft, 8 (KU). QUERETARO: Tequisquiapam, 12 (USNM). Dipodomys phillipsii perotensis Merriam 1894. Dipodomys perotensis Merriam, Proc. Biol. Soc. Washington, 9:111, 21 June. Type locality—Perote, Veracruz. 1944. Dipodomys phillipsii perotensis, Davis, J. Mamm., 25:391, 21 December. 69 May 1971 GENOWAYS AND JONES—SYSTEMATICS OF DIPODOMYS 283 Distribution—Known from Tlaxcala, a limited area in west-central Veracruz in the vicinity of the type locality, and from eastern Puebla (see Fig. 5). Remarks.—From D. p. phillipsii, the subspecies perotensis is distinguishable by its somewhat longer cranium (see Table 3), narrower maxillary breadth and _interorbital constriction, and paler dorsal coloration. Comparisons of perotensis with other subspecies are in the accounts of those taxa. Specimens from Tlaxcala (sample 11) are paler than specimens in the other two samples of perotensis studied, but in other respects the three samples are fairly homogeneous. Merriam (1893:86—88 ), quoting from the field notes of E. W. Nelson, stated that south- ern banner-tailed kangaroo rats were known from the northern and eastern base of Cerro de Malinche and from San Marcos, both places in Tlaxcala, and several localities in Puebla including Canada Morelos, Esperanza, San Juan de los Llanos, and Ojo de Agua. We have not seen specimens from any of these localities and it is unclear (except for the last- mentioned place) from the account whether Nelson had specimens in hand or simply based his notes on field observations. Nelson did see a specimen from Ojo de Agua, Puebla, in a small collection at a college in the city of Puebla. Specimens examined (67).—TLAXCALA: Huamantla, 3 (USNM). VERACRUZ: 2 km N Perote, 8000 ft, 1 (KU); 2 km W Perote, 8000 ft, 1 (KU); Perote, 7 (USNM); 2 km E Perote, 8300 ft, 7 (KU); Guadalupe Victoria (6 km SW Perote), 8300 ft, 5 (TCWC); 3 km W Limon, 7500 ft, 3 (KU); 2 km W Limon, 7500 ft, 4 (KU). PUEBLA: Laguna Salada (near Alchichia), S000 ft, 2 (TCWC): 2 km W Atenco de Aljojuca, 1 (UNAM); 10 km W Chalchicomula, 8300 ft, 1 (TCWC); Chalchicomula, 31 (USNM); 7 mi. S, 3 mi. E Puebla, 6850 ft, 1 (KU). Dipodomys phillipsii oaxacae Hooper 1947. Dipodomys phillipsii oaxacae Hooper, J. Mamm., 28:48, 17 February. Type locality— Teotitlan, 950 m, Oaxaca. Distribution—Known only from the type locality and one place in southern Puebla (see Fig. 5). Remarks.—This subspecies is easily distinguished from all others of the species by its small size. Also, the color of oaxacae is much paler than that found in populations in adjacent areas of Puebla and Veracruz. Specimens we have examined exhibit the narrow maxillary (88.3 per cent) and interorbital (56.8 per cent) breadths relative to mastoid breadth that is characteristic also of D. p. perotensis. D. p. oaxacae originally was described by Hooper (1947:48) on the basis of four specimens from Teotitlan, Oaxaca, until now the only known representatives of this distinctive sub- species. We have examined a specimen obtained by R. W. Dickerman at a place 1% mi. W Tehuitzingo, Puebla, on 15 August 1954 that also appears assignable to oaxacae (this is the single individual in sample 15). This specimen is a young adult, but its appear- ance does not suggest that it ever will attain the size of the larger perotensis, which occurs to the northeast. We regard this specimen as only tentatively assigned to oaxacae until additional material becomes available from southern Puebla. It extends the known range of the subspecies approximately 130 kilometers to the west-northwest. Specimens examined (5).—PUEBLA: 1% mi. W Tehuitzingo, 3570 ft, 1 (KU). OAXACA: Teotitlan, 950 m, 4 (UMMZ). NATURAL HISTORY Habitat Although there has been no extensive ecological study of the southern banner-tailed kangaroo rat, notes on natural history of the species have 70 284 JOURNAL OF MAMMALOGY Vol. 52, No. 2 appeared in several publications (Merriam, 1893:88-89; Davis, 1944:391; Villa-R., 1953:404; Dalquest, 1953:117; Baker and Greer, 1962:103; Hall and Dalquest, 1963:282-283). The accounts of Merriam and of Hall and Dalquest are especially noteworthy and both contain descriptions of the burrows of D. phillipsiit. Most of the accounts record these kangaroo rats as commonest on sandy soils in areas of short grass where large clumps of prickly pear or nopal cactus and low thornbrush are found. It is interesting to compare the record given by Merriam (op. cit.) of E. W. Nelson’s field accounts, written in 1892 and 1893, in which it was noted that the species was abundant in the vicinity of Tlalpam in the Valley of Mexico, and that given by Villa-R. (op. cit.), written in the early 1950's, in which it was stated that the species was scarce in the vicinity of Tlalpam; in fact, Villa was unable to obtain specimens from that area. Authors agree that this kangaroo rat is extremely difficult to trap, possibly accounting for Villa’s inability to obtain specimens, but an alternative is that the species may have been displaced from the vicinity of Tlalpam by urbanization. In the following paragraphs, we have given brief descriptions of seven representative localities at which D. phillipsii was obtained by field parties from the Museum of Natural History and for which field notes are available. These portray the situations in which this species may be found and list other species of mammals that may be expected to be found in association with the southern banner-tailed kangaroo rat. 8 mi. SE Zacatecas, 7225 ft, Zacatecas—R. H. Baker and a group of students visited this locality on 12-13 July 1952. Soils of the area are of volcanic origin and volcanic rocks were evident on the hills west of their campsite. Much of the land was under cultivation and many traps were placed along the edges of cornfields. Others were placed around clumps of grass and nopal cactus in a ravine near the camp. More than 190 mice were taken in 350 traps on the one night of trapping. Surprisingly, seven other species of heteromyid rodents were taken along with Dipodomys phillipsii—Perognathus flavus, P. hispidus, P. nelsoni, Dipodomys merriami, D. ordii, D. spectabilis, and Liomys irroratus. Other small mammals collected in this area included Thomomys umbrinus, Reithrodontomys fulvescens, R. megalotis, Peromyscus maniculatus, P. melanophrys, and Neotoma albigula. La Mesa Maria de Leon, 7400 ft, Jalisco —This locality, situated on a mesa approximately 1000 feet above the country immediately to the east, was visited from 21 to 24 June 1966 by P. L. Clifton and Genoways. The top of the mesa was a grassland supporting scattered oak trees, thus giving those areas not under cultivation a park-like appearance; the eastern edge of the mesa was steep and rock outcroppings were common there. Stands of trees and brush were much denser on the escarpment, with oak and manzanita being most abundant. Other species of mammals obtained at this place included Didelphis marsupialis, Sylvilagus floridanus, Lepus callotis, Spermophilus mexicanus, S. variegatus, Perognathus flavus, Peromyscus boylii, P. maniculatus, P. melanophrys, Sigmodon hispidus, Neotoma albigula, Urocyon cinereoargenteus, Spilogale putorius, and Mephitis macroura. 10 mi. NW Matanzas, 7550 ft, Jalisco —P. L. Clifton described the area northwest of Matanzas in mid-May 1966 as consisting of thousands of acres of unbroken grassland, with scattered patches of nopal cactus. Low stands of oaks grew on small hills scattered through the area. Other mammals collected were Sylvilagus floridanus, Lepus callotis, Spermophilus spilosoma, Thomomys umbrinus, Peromyscus difficilis, P. maniculatus, P. melanophrys, P. truei, Neotoma albigula, Canis latrans, and Spilogale putorius. a May 1971 GENOWAYS AND JONES—SYSTEMATICS OF DIPODOMYS 285 TaBLeE 6.—Distribution by month of capture of 220 southern banner-tailed kangaroo rats of three age classes. Month Juvenile Young Adult Total January — — — — February 1 1 1 3 March — — — — April 0 J 30 31 May 2 5 11 18 June i) 4 Bho} 39 July 1 9) 28 31 August 0 1 6 7 September 3 2 Val 16 October i 1 16 18 November 0 2) 6 8 December 15 10 24 49 2 mi. SW Matanzas, 7550 ft, Jalisco—dAs the above locality, this place was essentially an unbroken prairie with scattered clumps of nopal cactus and thornbrush. Many traps were placed under clumps of nopal, which were surrounded by grass and weeds. The following species were obtained along with southern banner-tailed kangaroo rats on 13-14 October 1965: Spermophilus spilosoma, Thomomys umbrinus, Perognathus flavus, P. hispidus, Peromyscus difficilis, P. maniculatus, Onychomys torridus, Sigmodon fulviventer, and Mephitis macroura. S mi. W Encarnacion de Diaz, 6000 ft, Jalisco—Vegetation in this part of Jalisco was primarily grassland, scattered with mesquite and other thorny bushes. Some cultivation (mostly corn) also prevailed. Traps were set along the edge of a cornfield and among weeds along a rock fence. Mammals obtained in the period 6 to 10 October 1965 included Sylvilagus audubonii, Spermophilus mexicanus, S. spilosoma, Perognathus flavus, P. hispidus, Dipodomys ordii, D. phillipsii, Reithrodontomys fulvescens, and Mus musculus. 4 mi. N, 5 mi. W Leon, 7000 ft, Guanajuato.—This locality was visited by R. H. Baker and his field party shortly after they visited the locality in Zacatecas discussed above. The party camped on a grassy hillside where thornbrush and nopal cactus were abundant. There were numerous rock fences in the area along which many traps were set. Other rodents trapped at this locality included Perognathus flavus, P. hispidus, Reithrodontomys fulvescens, Peromyscus maniculatus, P. melanophrys, P. truei, and Baiomys taylori. % mi. W Tehuitzingo, 3570 ft, Puebla—Vegetation west of Tehuitzingo was dominated by mesquite; some areas were under cultivation with the fields planted mainly to corn. R. W. Dickerman, a field representative of the Museum of Natural History, trapped on 15 August 1954 along a sandy river bed and among brush on the dry slope above the river. Aside from a single specimen of D. phillipsii, the only other small mammal obtained there was Liomys irroratus. Reproduction Of 27 adult female southern banner-tailed kangaroo rats that were examined for reproductive data, only three were found to contain embryos. A female taken on 1 June 1954 at the southeast end of Laguna de Santiaguillo, Durango, carried two embryos that measured 25 in crown-rump length, and two females obtained on 25 October 1950 at a place 1 mi. NE Villa Hidalgo, Jalisco, each contained three embryos that measured 16 (KU 40014) and 24 72 286 JOURNAL OF MAMMALOGY Vol. 52, No. 2 (KU 40015) in crown-rump length. The remaining females, mostly collected in the months of June, July, and August, evinced no gross reproductive activity, and Hall and Dalquest (1963:283) reported that no females taken in Veracruz from late September to mid-November were pregnant. Length of testes for three adult males were 9 (3 June), 12 (23 June), and 11 (15 August). Table 6 records 220 of the specimens we have examined by month of collection and by age. Only two months (January and March) are un- represented by specimens. In only three months—April, August, and Novem- ber—of the remaining 10 were no juveniles present in the sample and young individuals were present in all months. These data would seem to indicate a more prolonged reproductive period than can be deduced from the meager data on known reproduction in females. RESUMEN En un estudio de las ratas canguros del grupo Dipodomys phillipsii, se calcularon diversas variaciones geograficas y no geograficas. En la muestra proveniente de la vecindad de Perote, Veracruz, se reconocieron tres clases de edades (juveniles, subadultos, y adultos). En la muestra de Chalchicomula, Puebla, la variacion estadistica de los caracteres sexuales secundarios medidos fué poco significativa. Las variaciones geograficas de las medidas externas, craneales y del color del pelage fueron estudiados por medio de analisis de varianza y multivarianza para 15 muestras geograficas, las cuales revelaron que Dipodomys ornatus debe ser colocado como subespecie de D. phillipsii.. Otras razas validas son phillipsii, perotensis, y oaxacae. Se incluye también algunas notas sobre la morfologia del baculum, los lugares de vida y la reproducci6on de este grupo. LITERATURE CITED ALVAREZ, T. 1961. Sinopsis de las especies Mexicanas del genero Dipodomys. Revista Soc. Mexicana Hist. Nat., 21:391-424. ATCHLEY, W. R. 1970. AD OA 08 a6 oA do a0 Q4 OA @n Of na af On it XY 10 WV Dh AB ak an Qa an ase? AN RA AN 2a nn A488 we Ae AB Am AA AL AK OS Ai XY 1-32 Fics. P. melanotis. mi. E. Perote, Veracruz, Mexico, 2) Number 13677 collected from 29.1 mi. W. El Salto, Durango, Mexico, and 3) Number 13661 collected from the Santa Catalina Mountains, Pima County, Arizona. Representative karyotypes of male 1) Number 13684 collected from 4 Rasmussen, 1970; Savage and Cameron, 1971; Jensen and Rasmussen, 1971). The mountain top populations that have 30 acrocentric chromosomes differed from the other populations studied (Rasmussen, 1970; Jensen and Rasmussen, 1971) by having different gene frequencies and by being monomorphic for several loci where P. maniculatus is usually polymorphic. Our electrophoretic data are from a limited number of specimens (Table 2); however, most (80-90% )of the genetic variation in a species of Peromyscus can be detected in mice from a single population (Selander et al., 1971). On the assumption that the alleles in the Chiricahua populations were identical in both studies, our data are consistent with those of Rasmussen (1970) with one exception (Table 2). We did not detect the rare hemoglobin variant in the Chiricahua Mountain population. Albumin and transferrin are monomorphic and 86 J. H. BOWERS ET AL. DK SK BRAG AN AD AR AA” Am AR RA BA RK AAR KA AX Raw AX 10 v HE he Ah an | AN ER ARRA BAKy xa xa © KAM AN WRER AA ERAN RA RA KS AN AQOA aa ob AS AK AR BA AB hv aa aa © AR KK RA KK BA Avr Rm AK &* KA DN AN on ao aa ie ba XY Fics. 4-6. Representative karyotypes of male P. maniculatus. 4) P. m. fulvus, Number 10343 from 7 mi. S.S.E. of Perote, Veracruz, 5) P. m. rufinus, Number 13622 from Coconino County, Arizona, and 6) P. m. blandus, Number 13577 from 2.2 mi. S.E. Portal Cochise County, Arizona. hemoglobin essentially monomorphic in the populations from the Chiricahua, Pinaleno (sometimes referred to as the Graham Mountains) and Santa Catalina mountains, Arizona, and El Salto, Perote, and Dis- tricto Federal, Mexico. The various popu- lations of P. melanotis (the samples from Mexico) are identical to those of supposed P. maniculatus from southern Arizona in their albumin, transferrin and hemoglobin banding patterns. We also processed two individuals of P. maniculatus from near Portal, Arizona and three from the mountains near Flagstaff, Arizona. Exact allele designation in ac- cordance with Rasmussen’s designation is impossible for each allele without running comparison gels using his specimens. How- ever, it is probable that Trf-B, Trf-C and Alb-B and Alb-C were present at both locations as at least one mouse from each site was heterozygous for each system, and STUDIES OF DEER MICE 381 Fic. 7. Values enclosed in parentheses represent polymorphism in a single population. study and available literature. neither band corresponded to Alb-D and Trf-C of P. melanotis. All five P. manicu- latus were homozygous for the common hemoglobin allele in P. maniculatus. Neither albumen band corresponded to Alb-C and neither transferrin band cor- responded to Tri-C of P. melanotis. The probable explanation of this large amount of karyotypic and electrophoretic variation in presumed P. maniculatus is that more than one species is involved. We believe this to be the case concerning the forms from the Chiricahua, Pinaleno and Santa Catalina mountains of southern Arizona. A comparison of the karyotypes of P. melanotis from Perote, Veracruz (Fig. 1), and El Salto, Durango (Fig. 2), with that of P. maniculatus rufinus (Fig. 3) from Pima County, Arizona, reveals the three 87 Variation in the number of acrocentric chromosomes of P. maniculatus and P. melanotis. Data are from this karyotypes to be indistinguishable from each other. All populations of P. manicu- latus that have thirty acrocentrics are re- stricted to higher life zones (coniferous forest) of the isolated mountain ranges (Fig. 7). The lowland populations from southern Arizona have 10 acrocentrics. The ecological range of P. melanotis is restricted te the high coniferous forest of central and northern Mexico and its associated grasslands. That the similarity of habitat, karyotype and electrophoretic mobility patterns re- flect a true genetic relationship is also sup- ported by the results of breeding studies. Forty-two crosses have been attempted be- tween animals from the southern Arizona mountain populations having 30 acrocen- tric chromosomes with specimens of P. melanotis from Perote, Veracruz, Popo- 382 TABLE 2. J. H. BOWERS ET AL. Estimated allelic frequencies in montane populations of Peromyscus. Protein Alleles Albumins Transferrins Hemoglobins N A B Cc D E A B (G; A O Kaibab Plateau’ 85 0.01 0.04 0.95 0.01 0.01 0.81 0.18 0.61 £0.39 Flagstaff" 47 0.01 0.03 0.95 0.01 0.76 0.24 0.62 0.38 Mingus Mtn, I’ 24 0.02 0.17 O81 0.83 0.17 O69 O31 Mingus Mtn. I1' 34 0.04 0.96 0.63 0.37 O54 0.46 White Mtns., 1966’ Si O03 0.11 0.86 0.85 0.15 0.36 0.64 White Mtns., 1968' 18 0.14 0.83 0.03 0.72 0.28 0.42 0.58 White Mtns., 1969' 1S “O06, “OL 0:78 0.03 0.69 O28 0.61 0.39 Pinaleno Mtns.’ 56 1.00 1.00 1.00 Pinaleno Mtns. 2 1.00 1.00 1.00 Chiricahua Mtns." 62 1.00 1.00 1.00 0.06 Chiricahua Mtns. 9 1.00 1.00 1.00 Santa Catalina Mtns.’ 38 1.00 1.00 1.00 El Salto, Durango 3 1.00 1.00 1.00 Districto Federal 5 1.00 1.00 1.00 Perote 3 1.00 1.00 1.00 1 Data from Rasmussen (1970) and Jensen and Rasmussen (1971). cateptel, Districto Federal, and El Salto, Durango. Twenty-four of these attempted crosses were successful (57%). Successful crosses between individuals from each of three southern Arizona mountains (Chiri- cahua, Pinaleno and Santa Catalina) have been made with specimens of P. melanotis from each of the above mentioned localities. Attempted crosses of specimens from the southern Arizona mountain top popula- tions with 30 acrocentrics times P. manic- ulatus with 10 acrocentric elements (30 crosses attempted) collected from the low- lands of Arizona southeast of Portal and times individuals from the coniferous forest of the mountains of Arizona and New Mexico (58 crosses attempted) have failed to produce a single litter. Crosses made between individuals of P. melanotis from the same locality resulted in 33 of 77 at- tempted crosses being successful (437). Thus, the populations in southern Ari- zona isolated on the tops of the Chiri- cahua, Pinaleno and Santa Catalina mountains have 30 acrocentrics, are mono- morphic for Alb-D and Trf-C and do not 88 readily interbreed with other populations of P. maniculatus. These characteristics are the same as those of populations of P. melanotis from within its currently recog- nized distribution. Cross-fertility of the populations of P. melanotis with those of southern Arizona further argues their con- specific nature. Rasmussen (1970) argued that the rela- tively high degree of genetic monomorphism was due to drift in these isolated mountain populations. Our study suggests this is an artifact produced by combining data from two species, P. melanotis being mono- morphic and P. maniculatus polymorphic for the loci that happened to be studied. However, P. melanotis shows variability in other genetic systems that were not presented in his paper (e.g., phosphogluco- mutase-3). There is no evidence for the occurrence of genetic drift in these isolated mountain populations, and the danger of using only a limited number of loci and improper species identification should be apparent. Jensen and Rasmussen (1971) and Brown and Welser (1968) concluded STUDIES OF DEER MICE that albumin migration patterns would be of little or no taxonomic value. Our study and those of Smith et al. (1973) indicate this conclusion was premature and that albumin patterns may actually be quite useful. We have studied only a small part of the P. maniculatus complex, but certain karyotypic patterns have become evident and breeding studies have supported the genetic reality of these patterns. The agree- ment between karyotypic and _ electro- phoretic mobilities characteristic of these populations and the taxonomic lines sug- gested by the karyological and breeding data is impressive. Our study reveals that when preliminary data from a character obviously do not fit present taxonomic lines, it should not be concluded that the character will be of no apparent taxonomic or phylogenetic value. We believe that more intensive study of the karyotypes of P. maniculatus, (especially with hetero- chromatin and Giemsa banding techniques) taken in conjunction with breeding and electrophoretic studies, will result in a much better understanding of the evolu- tion and systematics of this species. Cer- tainly no character can be unconditionally accepted to imply a close phylogenetic rela- tionship. For instance, the karyotype of Peromyscus floridanus as published by Hsu and Arrighi (1968), is very similar to that shown for P. melanotis (Figs. 1-3). These two species are presently placed in separate subgenera, and we do not know if this similarity of karyotypes has resulted from convergent evolution or from both remain- ing unchanged since divergence from a common ancestor. The point is that this is only one character. As far as the relationship of P. manicu- latus to P. melanotis is concerned, we have no data to suggest natural hybridization. Further, none of the animals with 30 acro- centrics have been successfully crossed with any P. maniculatus from a southwest desert population or from the adjacent mountain populations of New Mexico or 89 383 Arizona. The one successful cross reported in the literature involved specimens from the Ann Arbor, Michigan, area times P. melanotis from El Salto, Mexico (Clark, 1966). One of our laboratory stocks is from El Salto, Durango, and, as indicated above, all crosses of this stock (16 at- tempted) times various P. maniculatus were negative. In Clark’s study (1966), only one of four attempted matings was suc- cessful, and this mating produced all males (Clark does not mention the number of young produced). It may be that in the zone where the two species have been in contact for some time, isolating mechanisms have evolved; however, where the two forms are more distantly associated from a geographical point, their isolating mech- anisms may not have been established. Also, this may represent an isolated in- stance of compatibility between the two species. If this cross is valid, it certainly suggests some interesting implications; however, additional work is in order be- fore we place too much importance on the data. Blair (1950:270) discussed the evolu- tion and speciation of P. maniculatus and related species. He concluded that species on the margins of the range of P. manicu- latus have resulted from ‘peripheral iso- lates” which have undergone ‘“‘both adap- tive and nonadaptive differentiation in morphological, physiological and psycho- logical characters.” Blair concluded that P. maniculatus was the parental stock that gave rise to melanotis, polionotus, sitkensis, slevini and sejugis. We agree with this interpretation. In addition, we feel that the preliminary data indicate that the P. maniculatus complex may closely fit the “centrifugal speciation” model proposed by Brown (1957) which involves the classical concept of adaptation of these groups to local conditions. A critical component of the ‘‘centrifugal speciation” hypothesis is that the center is the principal source of evolutionary change leading to “potential new species.” In our particular case, we 384 interpret “the center” to be the species Peromyscus maniculatus. In Brown’s model, the peripheral populations will be more primitive than the central stock, and it is possible that the peripheral populations may be more genetically compatible with each other than with the more rapidly evolving central stock. The following discussion will serve to show the relationship of our data to Brown’s model. 1) Hsu and Arrighi (1968) and Baker and Mascarello (1969) hypothesized that the primitive karyotype for Peromyscus was 48 with a large number of acrocentrics. In the P. maniculatus complex the popu- lations with higher numbers of acrocentrics are found in the peripheral isolates (Fig. 7) and in the more peripheral populations. Peromyscus melanotis has 30 acrocentrics; P. polionotus has 24-26 acrocentrics. In these two species, which are composed of numerous populations that are completely isolated from each other, only one minor chromosomal polymorphism and no chro- mosomal races have been described (Te and Dawson, 1971). When the chromo- somal data for these two species are con- trasted with the many races and _ poly- morphisms of P. maniculatus, one is forced to conclude that P. maniculatus is in a more dynamic evolutionary state. 2) Peromyscus melanotis is not genet- ically compatible with the nearest popula- tions (from the Mogollon rim, Arizona, or the Sacramento Mountains of New Mexico) or with its ecological equivalent, P. ma- niculatus rufinus or with the geographically adjacent grassland population P. manicu- latus blandus. Peromyscus melanotis will hybridize with P. maniculatus bairdii from Michigan (Clark, 1966). Bowen (1968) suggested that P. maniculatus bairdii gave rise to P. polionotis. Clearly additional data are needed. However, should the peripheral isolates and other peripheral populations be more genetically compatible with each other than with the central stock of P. maniculatus from the central U.S. J. H. BOWERS ET AL. and Mexico, then this complex will closely fit the model for centrifugal speciation. SUMMARY An unusual amount of chromosomal polymorphism and geographic variation in chromosomes and electrophoretic pattern have been reported for Peromyscus ma- niculatus. Karyological, electrophoretic and breeding data indicate that populations of Peromyscus from the Chiricahua, Pina- leno and Santa Catalina Mountains in southern Arizona are conspecific with P. melanotis, not with P. maniculatus. ‘These data also argue against the assumptions that monomorphism in the isolated popula- tions arose by drift. Rather they support a model of centrifugal speciation. ACKNOWLEDGMENTS We gratefully acknowledge Dr. Robert K. Selander for his criticisms and for usage of his laboratory. John Avise, Dale Berry, William Bleier, Joanne Bowers, Mark Bowers, Brent Davis, Genaro Lopez, Bob Martin, Kenneth Matoka, Rick McDaniel, Paul Ramsay, Jim Reichman, Sherry Shackelford, Gordon Smith, Melinda Smith and Bradley Wray assisted in collecting specimens and Ruth Barnard and Mike Jackson gave technical assistance. Sup- ported in part by a NSF Science Faculty Fellowship awarded to Bowers and NSF Grant GB 8120, NIH Grant GM-15769 and AEC Contract At(38-1)-310. APPENDIX Specimens Examined Peromyscus maniculatus: P. m. blandus Os- good. TEXAS: Jeff Davis County, 9.3 mi. W. Balmorhea on Texas 17, one female, 13580. ARIZONA: Cochise County, 6.5 mi. S.E. Portal, 3 males, 13567, 13573, 13575; 2.5 mi. S.E. Portal, eight males, 13564-13566, 13569, 13570, 13572, 13576, 13579, one female, 13574; 2.2 mi. S.E. Portal, 4 males, 13568, 13571, 13577, 13578. MEXICO: CHIHUAHUA: 47.2 mi. S. Jiminez, 2 males, not yet catalogued. ZACATECAS: 7 mi. E. Mazapil, one female, not yet catalogued. P. m. fulvus Osgood. MEXICO: VERACRUZ: 7 mi. S.S.W. Perote, one male, 10345, two females, STUDIES OF DEER MICE 10343, 10344. P. m. luteus Osgood. TEXAS: Andrews County, 18 mi. E. and 2 mi. N. Andrews, one male, 10393. Ector County, 10 mi. E. Odessa, one male, 10387. Hale County, 1.5 mi. W. Plain- view, 3 females, 13582-13584. 3.2 mi. N. Plain- view, 3 males, 10352, 10395, 13858, 8 females, 10359, 10360, 10362, 10363, 10386, 13587, 13588, 13586. Hardeman County, 2.5 mi. N.E. Quanah, 2 males, 10372, 13592, 6 females, 10370, 10371, 10385, 13589, 13590, 13591. Hockley County, 8.5 mi. N.W. of Levelland, two males, 10378, 10379, three females, 10377, 13593, 13594. Lamb County, 7.2 mi. S. Olton on F. M. 168, four males, 10366, 10382-10384, four females, 10364, 10365, 10380, 10381. Lubbock County, 0.5 mi. N. of Lubbock Lake Site, six males, 10368, 13597-13601, nine females, 10367, 10369, 13596, 13602-13607. Mc- Culloch County, 5 mi. S.E. Brady, two males, 10391, 10392, one female, 13595. OKLAHOMA: Texas County, 10 mi. E. Hardesty, one male, 10361. Washita County, 2 mi. W. Burns Flat, five males, 10373-10376, 13581. P.m. ozarkiarum Black. TEXAS: Wichita County, Spillway of Lake Wichita, Wichita Falls, one male and one female, uncatalogued. P. m. rufinus (Merriam). COLORADO: Larimer County, 13 mi. W. Ft. Collins, one male, 13623. Weld County, 25 mi. N.E. Ft. Collins, one male, 13624. NEW MEXICO: Taos County, Taos, two females, 13649, 13650. Torrance County, Red Canyon, Cibola National Forest, three males, 10357, 10358, 13651, two females, 10355, 10356. Lincoln County, 2 mi. W. Bonita Lake, Lincoln National Forest, five males, 10353, 13625, 10354, 13626, 13628, one female, 10350. Otero County, Cloud- croft, thirteen males, 13629-13632, 13635-13637, 13642-13646, 13648, five females, 13633, 13634, 13639, 13640, 13641. ARIZONA: Coconino County, 2 mi. E. U.S. Hwy. 89 on the Sunset Crater Road, fourteen males, 13609-13622. Peromyscus me- lanotis: Allen and Chapman. ARIZONA: Pima County, Santa Catalina Mountains, Bear Wallow Campground, one male, 13661. Graham County; Coronado National Forest, Arcadia Campground, two males, 13657, 13658, one female, 13660. 35.0 mi. W. junction of U.S. Hwy. 666 and Arizona 366, one male, 13659. Cochise County, 14 mi. W. Portal, four males, 13653-13656. MEXICO: CHIHUAHUA: 8.2 mi. S. San Juanita, one male, 13662, one female, 13663. DURANGO: 25.2 mi. W. El Salto, six males, 13664-13666, 13673, 13675, 13676, one female, 13674. 29.1 mi. W. El Saito, four males, 13677-13680. 31 mi. W. El Salto, four males, 13667, 13668, 13670, 13671, two fe- males, 13669, 13672. VERACRUZ: 4 mi. E. Perote, three males, 13682-13684, one female, 13681. DISTRICTO FEDERAL, 17.3 mi. S.E. Amecameca on the road to Popocatepetl, six males, 13686-13688, 13691-13693, two females, 13689, 13690. 91 385 The following specimens were processed elec- trophoretically and are preserved in the labora- tory of Dr. Robert K. Selander, Department of Zoology, The University of Texas at Austin. The specimens are identified by Dr. Selander’s labora- tory catalogue numbers: Peromyscus melanotis — ARIZONA: Graham County, Coronado National Forest, Arcadia Campground, 2(3615-16) ; Cochise County, 14 mi. W. Portal, 8(2404, 2410, 2415, 2420, 2422, 2426, 2430, 2432); MEXICO: DURANGO, 52 km W. El Salto, 3(3602-04); VERACRUZ, 7 km E. Perote, 3(3605—-7) ; DISTRICTO FEDERAL, 29 km S.E. Amecameca on the road to Popocatepetl, 3(3608-10); Fi hybrids, ARIZONA; Cochise County, 14.0 mi. W. Portal times MEXICO: Durango, 4(3611-14). LITERATURE CITED ARAKAKI, D. T., AnD R. S. Sparkes. 1967. The chromosomes of Peromyscus maniculatus hol- lesterit (deer mouse). Cytologic 32:180-183. ARAKAKI, D. T., I. VEoMETTI, AND R. S. SPARKES. 1970. Chromosome polymorphism in deer mouse siblings (Peromyscus maniculatus). Experientia 26:425-426. Baker, R. J. 1970. Karyotypic trends in bats, p. 65-96. In W. A. Wimsatt (ed.), Biology of Bats, Academic Press, London/New York. Baker, R. J., AND J. T. MAscareELio. 1969. Karyotypic analyses of the genus Neotoma (Cricetidae, Rodentia). Cytogenetics 8:187- 198. Birpsatt, D. A., J. A. RepFietp anp D. G. CAMERON. 1970. White bands on starch gels stained for esterase activity: A new poly- morphism. Biochemical Genetics 4:655-658. Brain, W. F. 1950. Ecological factors in the speciation of Peromyscus. Evolution 4:253- Zuo: Bowen, W. W. 1968. Variation and evolution of gulf coast populations of beach mice, Pero- myscus polionotus. Bull. Fla. State Mus. 12: 1-91. BrapsHaw, W. N., AND W. W. Gerorce. 1969. The karyotype in Peromyscus maniculatus nubiterrae. J. Mamm. 50:822-824. Brown, J. H., anp C. F. WeELserR. 1968. Serum albumin polymorphisms in natural and labora- tory populations of Peromyscus. J. Mamm. 49:420-426. Brown, W. L., JR. 7. Centrifugal speciation. Quart. Rev. Biol. 32:247-277. CanHAM, R. P., D. A. BrirpsaLt anv D. G. CAMERON. 1970. Disturbed segregation at the transferrin locus of the deer mouse. Genet. 195 ag Res. 16:355-357. Crark, D. L. 1966. Fertility of a Peromyscus maniculatus X Peromyscus melanotis cross. J. Mamm. 47:340. 386 Durrey, P. A. 1972. Chromosome variation in Peromyscus: A new mechanism. Science 176: 1333-1334. Hatt, E. R., ann K. R. Ketson. 1959. The mammals of North America. The Ronald Press Co., New York, Vols. 1 and 2. Hsu, T. C., anp F. E. Arricut. 1968. Chromo- somes of Peromyscus (Rodentia, Cricetidae). I. Evolutionary trends in 20 species. Cyto- genetics 7:417-446. JENSEN, J. N., ano D. I. Rasmussen. 1971. Serum albumins in natural populations of Peromyscus. J. Mamm. 52:508-514. Kine, J. A. (ed.). 1968. Biology of Peromyscus (Rodentia). American Society of Mammal- ogists, Special Publication No. 2. KREIZINGER, J. D., anp M. W. SuHaw. 1970. Chromosomes of Peromyscus (Rodentia, Cricet- idae). II. The Y chromosome of Peromyscus maniculatus. Cytogenetics 9:52—70. Oxuno, S., D. WerLER, J. Poore, L. Curistian AND C. StTentus. 1966. Autosomal poly- morphism due to pericentric inversions in the deer mouse (Peromyscus maniculatus) and some evidence of somatic segregation. Chro- mosoma 18:177-187. Patton, J. L. 1967. Chromosome studies of certain pocket mice, genus Peroguathus (Ro- dentia—Heteromyidae). J. Mamm. 48:27-37. Rasmussen, D. I. 1964. Blood group poly- morphism and interbreeding in natural popu- lations of the deer mouse, Peromyscus manicu- latus. Evolution 18:219-229. 1968. Genetics in biology of Peromyscus (Rodentia), p. 340-372. In King, J. A. (ed.), Publ. 2, American Society of Mammalogists. 92 J. H. BOWERS ET AL. 1970. Biochemical polymorphisms and genetic structure in populations of Peromyscus. Symp. Zool. Soc. Lond. 26:335-349. Rasmussen, D. I., J. N. JENSEN anp R. K. KoEeuHn. 1968. Hemoglobin polymorphism in the deer mouse, Peromyscus maniculatus. Bio- chemical Genetics 2:87-92. Rasmussen, D. I., ano R. K. KoEenn. 1966. Serum transferrin in polymorphism in the deer mouse. Genetics 54:1353-1357. SavacE, E., anp D. G. Cameron. 1971. Blood group complexity: the Pm locus in Peromys- cus maniculatus. Anim. Blood Groups Bio- chem. Genet. 2:23-29. SELANDER, R. K., M. H. Smith, S. Y. Yanc, W. E. Jounson anv J. B. Gentry. 1971. Bio- chemical polymorphisms and systematics in the genus Peromyscus. I. Variation in the old- field mouse (Peromyscus polionotus). Studies in Genetics VI. Univ. Texas Publ. 7103:49- 90. SincH, R. P., anno D. B. McMutran. 1966. Karyotypes of three subspecies of Peromyscus. J. Mamm. 47:261-266. SmitH, M. H., R. K. SELANDER, W. E. JoHNSON AND Y. J. Kim. 1973. Biochemical poly- morphism and systematics in the genus Pero- myscus. III. Variation in the Florida deer mouse (Peromyscus floridanus), a Pleistocene relict. J. Mamm. 54:(in press). SPARKES, R.S., anpD R.S. ARAKAKI. 1966. Intra- subspecific and intersubspecific chromosomal polymorphism in Peromyscus maniculatus (deer mouse). Cytogenetics 5:411-418. Te, G. A., anD W. D. Dawson. 1971. Chromo- somal polymorphism in Peromyscus polionotus. Cytogenetics 10:225-234. A MULTIVARIATE ANALYSIS OF SYSTEMATIC RELATIONSHIPS AMONG POPULATIONS OF THE SHORT-TAILED SHREW (GENUS BLARINA) IN NEBRASKA Hucu H. Genoways AND JERRY R. CHOATE Abstract Genoways, H. H., and J. R. Choate (Museum of Natural History, The Univ. Kansas, Lawrence, Kansas 66044. Present addresses: The Museum, Texas Tech University, Lubbock, Texas 79409 and Division of Biological Sciences and Agriculture, Fort Hays Kansas State Col- lege, Hays, Kansas 67601). 1972. A multivariate analysis of systematic relationships among populations of the short-tailed shrew (genus Blarina) in Nebraska. Syst. Zool., 21:106-116.— The genus Blarina (Mammalia: Soricidae) is represented in Nebraska by two well-dif- ferentiated, geographically exclusive phena that generally have been regarded as subspecies. Field studies conducted along their zone of contact resulted in the collection of represent- atives of both phena at each of five localities. Cluster analysis of distance matrix readily separated reference samples of the phena as well as test samples from near the zone of contact. A three-dimensional projection of the specimens onto their first three principal components, together with a discriminant function analysis, served further to elucidate the degree of differentiation among the phena and to confirm that their characteristic differences are maintained even where they occur sympatrically. The latter technique also indicated that one specimen not singled out by other analyses might be a natural hybrid, but none of the analyses provided even the slightest evidence for panmictic intergradation. The possibility that the phena represent the ends of a circularly inter- grading species is considered, as is the possibility that the phena are distinct, biological species. Two means of speciation, one “classical” and the other involving formation of “stasipatric species,” are discussed. tions; Hybridization. ] Shrews of the Nearctic genus Blarina (Mammalia: Soricidae) historically have been classified as representatives of two species—one, B. brevicauda (Say), wide- ranging and geographically variable, and the other, B. telmalestes Merriam, re- stricted to the Dismal Swamp region of coastal Virginia and North Carolina and of uncertain taxonomic status (see Hall and Kelson, 1959:53, 55). This arrangement stems primarily from Merriam’s (1895) re- vision of Blarina and Bole and Moulthrop’s (1942) later synopsis of the genus. As presently understood, the ranges of four nominal subspecies—B. b. brevicauda, B. b. kirtlandi Bole and Moulthrop, B. Db. churchi Bole and Moulthrop, and B. b. talpoides (Gapper)—all characterized by large external and cranial dimensions, geographically abut the range of B. b. carolinensis (Bachman), which is char- acterized by much smaller size. This zone of contact extends from Nebraska to Mary- [Multivariate analysis; Systematics; Blarina; Popula- land and effectively divides the range of the species into two parts—a northern seg- ment occupied by comparatively large shrews and a southern segment occupied by smaller shrews (Hall and Kelson, 1959: 53). Jones and Findley (1954), and sub- sequently Jones and Glass (1960), studied the geographic relationships of taxa of Blarina west of the Mississippi River. They demonstrated the presence of a clinal in- crease in size from the Gulf coastal region to northern Nebraska. The cline exhibited a significant “step” in southern Nebraska, which was considered to constitute the line of demarcation between B. b. brevicauda and B. b. carolinensis. The magnitude of the “step” is such that Nebraskan speci- mens of B. brevicauda invariably can be assigned to subspecies without regard for location of capture; external and cranial dimensions in B. b. brevicauda are sub- stantially greater than (and seldom over- 106 93 BLARINA IN NEBRASKA 107 lap) those in B. b. carolinensis (Jones, 1964:67, 69, 72). Jones (1964:67) found no specimens from Nebraska that could be described as exactly intermediate between brevicauda and carolinensis, and (1964:28 ) regarded the two phena as “markedly dif- ferent subspecies . . . that now meet along a fairly well-defined line in Nebraska with little intergradation between them.” The geographic relationship of large northern taxa to small southern taxa of Blarina apparently has remained un- changed, except for latitudinal shifts in position, for a long period of time. Par- malee (1967:135-136) reported two dis- tinctive phena of Blarina in a Recent bone deposit in Illinois; Oesch (1967:171) found the two phena in a Pleistocene (late Wis- consin) deposit in Missouri; and Guilday et al. (1964:147-151) described large and small phena of Blarina from Pleistocene (Wisconsin) deposits in Pennsylvania and Virginia. These findings generally have been interpreted to demonstrate _ that climatic fluctuations have effected se- quential geographic replacement of one subspecies by another although, as Par- malee (1967:136) admitted, “it is problem- atical as to whether these races were contemporaneous or occupied the [areas] during different periods.” Hibbard (1970:423) treated the two phena as dis- tinct species in earlier (Illinoian) Pleisto- cene deposits, and preliminary cytogenetic studies (Elmer C. Birney, personal com- munication; Meylan, 1967; Lee and Zim- merman, 1969:337; Hoffman and _ Jones, 1970:389) have indicated that, indeed, more than one species might be involved (brevicauda has 48-50 chromosomes and carolinensis 46). The initial purpose of this study, there- fore, was to search the zone of contact between the nominal subspecies B. b. brevicauda and B. b. carolinensis in Ne- braska (see Jones, 1964:66) for evidence of intergradation or hybridization, and thereby to shed light on the systematic relationships of these taxa. 94 METHODS AND MATERIALS Intermittent field studies were conducted in the period 1965 to 1969 in three areas of Nebraska where the ranges of B. b. brevicauda and B. b. carolinensis were thought to be contiguous (see also Choate and Genoways, 1967; Genoways and Choate, 1970). One area in northeastern Adams and northern Clay counties was selected because a specimen identified as carolinensis had been obtained previously by Genoways at a place 1% mi. N and 6 mi. E Hastings, Adams County, and Jones (1964:68) had reported one specimen of brevicauda from just 18 miles to the east at Saronville, Clay County. Additional col- lecting indicated that the zone of contact was between Harvard and Saronville in northern Clay County, and specimens ten- tatively identified as brevicauda were caught together with specimens of caro- linensis at each of three localities (1 mi. N and 3 mi. W Saronville; 1 mi. N and 2 mi. W Saronville; 1 mi. N and 1 mi. W Saron- ville). At the first two localities repre- sentatives of both taxa were taken together in the same traplines on 20 December 1965, whereas at the last locality a specimen identified in the field as brevicauda was caught on 20 November 1965 and a speci- men identified as carolinensis was taken on 2 April 1966. In eastern Saline County the two taxa also were known from only 18 miles apart (brevicauda from 4 mi. NE Crete and carolinensis from 1% mi. W De Witt). We were unable to define the exact area of contact in Saline County, but the known distance between the taxa was reduced to seven miles with the capture of a speci- men tentatively identified as carolinensis at a place 5 mi. S and 3 mi. E Crete. The third area in which field studies were conducted was in Cass County, which was selected because a specimen definitely identified as brevicauda was known from just north of the county line at a place 1 mi. W Meadow, Sarpy County, and two undoubted specimens of carolinensis had been reported previously (Jones, 1964:70) 108 SYSTEMATIC ZOOLOGY (en a So Se ee oe ee rl ] Museum of Natural History University of Kansas 1952 a 97 24-5648 Fic. 1—Map of Nebraska showing distribution of the brevicauda (half solid circles) and carolinensis (solid circles) phena of Blarina (modified from Jones, 1964:66). Localities plotted are those from which specimens were drawn for reference samples (see text). The shaded areas are enlarged in Fig. 2. from the county to the south (1 mi. SE Specimens thus collected (together with Nebraska City, Otoe County); furthermore, a few reported from near the zone of Jones (1964:67) assigned five specimens contact by Jones, 1964) were tested against from Louisville (in extreme northern Cass reference samples from Nebraska of brevi- County ) to B. b. brevicauda, but remarked cauda and carolinensis. Localities of refer- that they “are smaller externally and aver- ence samples in the following lists are ar- age slightly smaller cranially than topo- ranged from north to south and correspond types of that subspecies... .” By trapping to localities plotted in Figure 1; localities along a transect extending southward from oo, counties at about the same latitude are Louisville to a place just south of Weeping isted from west to east. Numbers in Water, we were able to locate the zone of parentheses indicate how many specimens contact between the two taxa. On 24 No- f ; oy: ; rom each locality were included in vember 1968, three specimens (one tenta- tively identified as en Se two as analyses. Numbers (bold face) of test carolinensis) were caught together in the samples refer to localities numbered in same trapline at a place 1 mi. S and 1% Figure 2. mi. W Weeping Water. In addition, two specimens identified in the field as brevi- cauda were caught on the same morning CHERRY CO.: 3 mi. SSE Valentine (1). at a place 2 mi. N and 2 mi. W Weeping KEYA PAHA CO.: 12 mi. NNW Spring- Water, and four specimens of brevicauda view (1). BOYD CO.: 5 mi. WNW Spen- and 27 of carolinensis were caught at other cer (1). HOLT CO.: 1 mi. S Atkinson (1); localities in the same area. 6 mi. N Midway (1). KNOX CO.: 3 mi. brevicauda reference sample 95 BLARINA IN NEBRASKA 96°15" 96°00' T PLATTE RIVER (J) SPRINGFIELD a eae ASHLAND [4 | MEADOW | 2@ 4 4 S bia CO OUIsVIILE @4 5@0 MANLEY PLATTSMOUTH ( \ MISSOURI RIVER 41°00" @6 7® @8 9° (> WEEPING WATER @e11 10 @12 ( a ee ae ee SCALE IN MILES DE WITT earolinenus es ts Ney Bere eer | reference 1 1 ' SCALE IN MILE s 96°15 96°00 L | 97°00 98°15 98° | HARVARD ' J) 19 22 UTTON HASTINGS ; ee Pee eee Jp — 18 if 20 mM 23, al I es e e ¢ Se =) 15@) o INLAND e i! i | 18 SARONVILLE | | aes: 0°35 ur ° st 40°35 i] ' | P [TP ccay CENTER | Se are ( | sc IN és ' L_ 1 Fic. 2.—Areas in eastern Nebraska where two phena of Blarina were found to be contiguous or sym- patric. A, Cass County and adjacent parts of southern Saunders and Sarpy counties; B, eastern Saline County; C, northeastern Adams County and northern Clay County. Numbered localities refer to test samples identified in text. Unnumbered localities indicate places where specimens of Blarina have been taken that could not be used in statistical analyses because we were unable to obtain some measure- ments from them. W Niobrara (1). CEDAR CO.: 4 mi. SE Laurel (6). WAYNE CO.: % mi. W Wayne (2); Wayne (7). BURT CO.: 1 mi. E Tekamah (2). VALLEY CO.: 2% mi. N Ord (2). WASHINGTON CO.: 6 mi. SE Blair (4). BUTLER CoO.: 4 mi. E Rising City (1); 5 mi. E Rising City (2). DAWSON CO.: 5 mi. S Gothenburg (1). HALL CO.: 6 mi. S Grand Island (1). (3). 2 ] 1 SEWARD CO.: 1 mi. N Pleasant Dale (3 96 carolinensis reference sample LINCOLN CO.: 2 mi. N North Platte (3). OTOE CO.: 3 mi. S, 2 mi. E Nebraska City (6). SALINE CO.: % mi. W De Witt (1). DUNDY CO.: 5 mi. N, 2 mi. W Parks (18). RICHARDSON CO.: 4 mi. E Barada (4); 5 mi. N, 2 mi. W Humboldt (2); 3% mi. S, 1 mi. W Dawson (3); 8 mi. S, 1 mi. E Dawson (1); 6 mi. W Fall City (1); % mi. S, 1% mi. W Rulo (2). 110 SYSTEMATIC ZOOLOGY Test samples 1—2 mi. NE Ashland, Saunders Co. (3). 2—1 mi. W Meadow, Sarpy Co. (1). 3— Louisville, Cass Co. (4). 4—% mi. N Man- ley, Cass Co. (1). 5—% mi. W Manley, Cass Co. (2). 6—2 mi. N, 2 mi. W Weeping Water, Cass Co. (2). 7—1 mi. N, 2 mi. W Weeping Water, Cass Co. (6). 8—%o mi. N, 2 mi. W Weeping Water, Cass Co. (1). 9—*%o0 mi. S, 2 mi. W Weeping Water, Cass Co. (10). 10—1 mi. S, 2 mi. W Weeping Water, Cass Co. (3). L1—1 mi. S, 1% mi. W Weeping Water, Cass Co. (3). 12—2 mi. S Weeping Water, Cass Co. (8). 13—2 mi. NE Crete, Saline Co. (3). 14—5 mi. S, 3 mi. E Crete, Saline Co. (1). 15—1% mi. N, 6 mi. E Hastings, Adams Co. (2). 16 —1%o mi. N, 5%o0 mi. E Hastings, Adams Co. (2). 17—% mi. N Inland, Clay Co. (1). 18—1 mi. S Harvard, Clay Co. (3). 19— 1% mi. E Harvard, Clay Co. (3). 20—1 mi. N, 6 mi. W Saronville, Clay Co. (1). 21— 1 mi. N, 3 mi. W Saronville, Clay Co. (3). 22—1 mi. N, 2 mi. W Saronville, Clay Co. (2). 23—1 mi. N, 1 mi. W Saronville, Clay Co. (2). Specimens listed above are housed in The University of Kansas Museum of Natural History. The age of each in- dividual selected for analysis was estimated (Choate, 1968:253; 1970:214), and no speci- men judged to be less than adult size was included in reference or test samples. Nine cranial measurements (Choate, 1972) were taken from each specimen by Choate (by means of dial calipers) as follows: occipito- premaxillary length; length of P4-M3; cra- nial breadth; breadth of zygomatic plate; maxillary breadth; interorbital breadth; length of mandible; height of mandible; articular breadth. Computations were performed using a system of multivariate statistical computer programs (NT-SYS) developed by F. J. Rohlf, R. Bartcher, and J. Kishpaugh for the GE 635 computer at The University of Kansas (see Schnell, 1970:42). Matrices of Pearson’s product-moment correlations were computed, and taxonomic distance coefficients were derived from standard- ized character values. Cluster analyses were conducted using UPGMA (un- weighted pair group method using arith- metic averages) on the correlation and distance matrices, and a phenogram was generated for each. Phenograms were com- pared with their respective matrices, and a coefficient of cophenetic correlation was computed for each comparison. A matrix of correlation among characters then was computed, and the first three principal components extracted. A three-dimensional projection of the OTUs onto the first three principal components was made; this pro- jection then was drawn using a Benson- Lehner incremental plotter. Rising (1968, 1970) used principal component analysis to assess interbreeding between species of chickadees (genus Parus) and _ orioles (genus Icterus), respectively. Discriminant function analysis was per- formed using the MULDIS subroutine of the NT-SYS system. This program uses variance-covariance mathematics to dif- ferentially weight characters relative to their within- and between-groups variation. For the discriminant analysis in this paper, two reference samples from areas geo- graphically removed from zones _ of suspected hybridization were used. A dis- criminant multiplier was calculated for each character, and this was multiplied by the value of its respective character; all such values were summed for each_ in- dividual to yield its discriminant score. The discriminant scores were plotted on a frequency histogram to compare in- dividuals of the two reference samples and to compare the test sample from the inter- mediate geographical areas where hybrid- ization was suspected. A good discussion of discriminant functions is given by Jolicoeur (1959); Lawrence and Bossert (1969) used this test to identify hybrids in their study of members of the genus Canis as did Birney (1970) in a study of woodrats of the genus Neotoma. o7 BLARINA IN NEBRASKA pu! RESULTS A distance phenogram (Fig. 3) was pre- pared using 21 reference specimens of B. b. brevicauda and 18 of B. b. carolinensis, together with 44 test specimens from lo- calities at or near the zone of contact of those taxa in Saunders, Sarpy, and Cass counties (Fig. 2A). The phenogram is divided into two major clusters separated by an appreciable phenetic distance (1.82). The upper cluster contains all the reference specimens of brevicauda, whereas the lower cluster contains all the reference specimens of carolinensis; specimens from test samples appear in both clusters. All specimens from as far south in Cass County as sample 6 are in the upper part with the brevicauda reference sample. Specimens denoted by an asterisk (6* and 12*) are discussed below. The six specimens from sample 7 and the 10 from sample 9 fall in the lower cluster with the reference speci- mens of carolinensis; however, a specimen from a geographically intermediate locality (sample 8) fell with the brevicauda speci- mens. Of the three specimens from sample 12 11, two are in the lower part with caro- C linensis, whereas the third is in the upper Ms part with brevicauda. All eight specimens 9 from sample 12 and the three from sample 10 are grouped with carolinensis. The two reference specimens of brevicauda at the lower end of the upper cluster of the phenogram, and at a substantial “distance” from other specimens in that group, are young adults with relatively small di- mensions. A three-dimensional projection of the specimens onto the first three principal ay * onn CNIA=NDWBDOMUMAOPF WU - DOD MDYNYUBDDTO“-DHO-DVDTOWODOD = ABONNALANANGN CN 7 9 c 9 7 — c 7 i c Fic, 3.—Phenogram computed from distance iS matrix based on standardized characters and clus- 9 tered by the unweighted pair-group method using E arithmetic averages (UPGMA). Numbers refer "1 to individuals from test samples identified in text |_____ 13+ and in Fig. 2. Specimens labelled “B” are from u reference samples of brevicauda, whereas speci- c mens labelled “C” are from reference samples of 7 carolinensis. An asterisk indicates that special ref- pe fe eee : : : M6) 149 133 119 1,05 091 0.79 063 O49 erence is made to the specimen in text. 98 112 BRS Lf ¥, , t D | eT hes I SYSTEMATIC ZOOLOGY rT AR ca mo ws Fic. 4.—Three-dimensional projection of 83 specimens onto the first three principal components based on a matrix of correlations among 12 external and cranial measurements. I and II are indicated in the fig- ure and III is represented by height. The first three components include approximately 92 per cent of the total variance, with component I accounting for 83.92, II for 4.88, and III for 3.15 per cent, re- spectively. Numbers refer to individuals from test samples identified in text and in Fig. 2. An asterisk indicates that special reference is made to the specimen in text. components (Fig. 4) likewise shows two groups, one (on the right in the figure) containing all the reference specimens of carolinensis and the other (on the left) all the reference specimens of brevicauda. One specimen from sample 12 (designated 12* ) is situated between the groups, as would be expected of a hybrid or intergrade, al- though it was grouped with the caro- linensis reference specimens in the distance phenogram. However, a note made by us when that specimen was measured suggests that it may have abnormal proportions (“skull unusually long, rostrum barrel- shaped, cranium narrow. relative to length”). The remainder of the specimens are clustered as would be expected on the basis of the distance phenogram. Note that the three specimens from locality 11 still are divided with two in the carolinensis cluster and one in the brevicauda cluster. Also, note the position of specimen denoted as 6* toward the lower limit of the brevi- cauda group; this specimen is discussed below. Discriminant function analysis (Fig. 5) was conducted using reference specimens totaling 37 for brevicauda and 40 for caro- linensis. From the table of discriminant multipliers (Table 1), it can be seen that 99 all the cranial measurements excepting length of the mandible were weighted heavily, whereas the three extemal mea- surements were weighted comparatively lightly. The discriminant scores for the brevicauda reference sample ranged from 38.158 to 43.330 and those for the caro- linensis reference sample ranged from 31.199 to 34.827, thus yielding a separation between the taxa of 3.331. The specimen (12*) that fell in the intermediate area of the three-dimensional plot (Fig. 4) has a TABLE 1. DISCRIMINANT MULTIPLIERS RESULTING FROM A DISCRIMINANT FUNCTION ANALYSIS COMPARING Blarina brevicauda brevicauda witH B. b. carolinensis In NEBRASKA. Discriminant Character Multiplier Total Length 0.045 Length of Tail Vertebrae —0.239 Length of Hind Foot 0.274 Occipito-premaxillary Length —0.482 Length of P4-M3 3.814 Cranial Breadth 1.023 Breadth of Zygomatic Plate —0.358 Maxillary Breadth —2.709 Interorbital Breadth 0.529 Length of Mandible 0.068 Height of Mandible 2.302 Articular Breadth 3.941 BLARINA IN NEBRASKA 113 REFERENCE CAROLINENS!IS =~ NW FU FADO BREVICAUDA REFERENCE Fic. 5.—Histogram of linear discriminant scores for short-tailed shrews from Nebraska. T T 37.4 38.2 Discrim- inant scores are indicated along the bottom of the histogram and frequency of individuals is indicated on the left-hand side. Individuals arranged below are from reference samples of brevicauda, at right, and carolinensis, at left. Individuals arranged above are numbered according to test samples, which are identified in text and in Fig. 2. value of 34.027 and clearly pertains to carolinensis. However, two test specimens from Cass County have values between those of the reference samples, as would be expected of hybrids or intergrades (see especially Lawrence and Bossert, 1969, and Birney, 1970). One of those specimens (from sample 12) has a value of 35.034 and probably is best considered a representa- tive of carolinensis. The other specimen (6*), with a discriminant score of 36.070, might actually be a hybrid between the taxa. It is of special interest to note that the discriminant score of this specimen was nearer the upper limit for carolinensis than the lower limit for brevicauda, although in both the distance phenogram and _three- dimensional plot (Figs. 3 and 4) the speci- men was grouped with brevicauda. Other specimens from Saunders, Sarpy, and Cass counties were arranged within the same phena as they were in the distance pheno- gram and three-dimensional plot; this in- cludes those from sample 11, where two specimens fell with the carolinensis refer- ence sample and one fell with brevicauda. The specimens denoted by an asterisk are discussed in text. From Saline County (Fig. 2B), the one specimen comprising sample 14 had a dis- criminant score that fell within the range of the carolinensis reference sample, whereas the three specimens from sample 13 all fell within the range for brevicauda. Among Clay County (Fig. 2C) specimens, three samples (21, 22, and 23) include representatives of both taxa, thus con- firming tentative field identifications. How- ever, at none of those localities or any other locality from which we have examined specimens is there any indication of inter- gradation between the taxa. DISCUSSION Data presented herein yield no_ indi- cation that the nominal subspecies B. b. brevicauda and B. b. carolinensis inter- grade in Nebraska. Only one specimen (6*, Fig. 5) was found to be intermediate between the phena using discriminant function analysis; a second possibly inter- mediate specimen (12*) was identified using the principal components analysis. Probably only the specimen from sample 100 114 SYSTEMATIC ZOOLOGY 6 is a “hybrid” or “intergrade” among the 66 specimens tested from the zones of con- tact between the two taxa. In other words, brevicauda and carolinensis behave as good biological species where their ranges are contiguous in southern Nebraska. Unpub- lished data (John B. Bowles, personal communication) indicate that a similar relationship between large and small phena of Blarina probably exists across southern Iowa. Panmictic intergradation resulting in numerous viable hybrids between brevi- cauda and carolinensis almost certainly does not occur west of the Mississippi River at the present time, and we know of no conclusive published evidence for inter- gradation east of the Mississippi River. That an occasional viable hybrid might be produced in the zone of contact between the phena is entirely consistent with their behavior as “species.” We recognize two possible explanations for the evolutionary relationship between these phena: (1) that they are an example of circular overlap (as defined by Mavr, 1963:507-512, 664) within the same species —this has been reported for several species of mammals, including Sorex vagrans (Findley, 1955:14), Thomomys_ talpoides (Long, 1965:603), and Peromyscus mani- culatus (Dice, 1931; Hooper, 1942; King, 1948; Harris, 1954)—or (2) that the phena represent distinct species as suggested by Hibbard (1970:423). Jones (1964:28-31) provided an expla- nation for the circumstances that might have resulted in Nebraskan populations of B. brevicauda becoming the ends of a circularly intergrading species. He hy- pothesized that B. brevicauda, which is a common inhabitant of the eastern decidu- ous forest, became widespread on_ the plains during the warm, wet segment of the Hypsithermal Period during _ post- Wisconsin times. The species probably varied clinally in size, ranging from small in the south to large in the north in typical Bergmannian fashion. During the sub- sequent Xerothermic Period, a_ general drying occurred and the distribution of B. brevicauda was divided into two segments as far east as the eastern limit of the so- called “prairie peninsula.” Jones postulated that during reinvasion of the plains those populations to the northeast and southeast reached Nebraska sooner than those di- rectly to the east; as a result, the middle portion of the cline was obliterated and two distinctly divergent phena achieved secondary contact. One notable characteristic of the ex- amples given for circular overlap that is lacking in Blarina is a high degree of ecological separation between the over- lapping subspecies (defined as “microallo- patry” by Smith, 1965:57). No ecological separation of the taxa is evident in Blarina in that all specimens from the zone of contact were trapped in grassy roadside ditches in otherwise highly agricultural areas; disruption of the original habitat, however, may have altered some original ecological differences. Another problem with this interpretation has to do with the fossil record; if available paleontological evidence is correct, the secondary zone of contact between the phena has fluctuated with regard both to latitude and longitude at least since the middle Pleistocene, long before the period of time suggested by Jones (1964) for elimination of the central part of the cline. Considering the element of time and the durability of the geographic relationship, the two taxa seem to us to be behaving more nearly like closely related species than like subspecies. If, indeed, the phena represent distinct species, speciation classically would be interpreted as having resulted from geo- graphic isolation of the phena during or before the Kansas glaciation, with the resultant taxa having maintained a_para- patric distribution (in the sense used for mammals by Vaughan, 1967, although pos- sibly without ecological divergence) at least since Illinoian times. Accordingly, the two species might have displaced one another north and south (and_ probably also east and west) across the plains in response to fluctuations in environmental 101 BLARINA IN NEBRASKA 115 factors during the Pleistocene, with one species competitively excluding the other depending on the direction of the climatic shift. Another possible interpretation is that the large and small phena of Blarina repre- sent “stasipatric species” (Key, 1968; White, 1968; White et al., 1967). With development of a “tension zone,” possibly as the result of the chromosomal differences between the two emergent phena, speci- ation might have occurred gradually with- out actual geographic isolation of the main body of the parental stock, although small peripheral populations undoubtedly must have undergone isolation and differentia- tion in the classical sense. The tension zone could have shifted position geographically, as described by Key (1968), in response to changing environmental conditions in the Pleistocene. Hybridization would have oc- curred regularly across the tension zone, especially early in the evolution of this complex. However, divergence now might have progressed to the level (at least in Nebraska) at which the tension zone of intergradation has ceased to function; the presence of only one probable hybrid in our combined samples of 66 specimens from at or near the zone of contact between the two phena strongly suggests that iso- lating mechanisms are actively preventing, or at least restricting, hybridization, and that introgression is negligible. ACKNOWLEDGMENTS Field studies conducted by the authors were supported in part by a grant from the Kansas Academy of Science. Multivariate analyses were performed on the GE 635 computer at The University of Kansas Computation Center. Joyce E. Genoways provided clerical assistance and prepared the illustrations. Finally, helpful discus- sions were held with numerous persons at The University of Kansas Museum of Natural History, but special thanks is due Drs. Elmer C. Birney, John B. Bowles, Robert S. Hoffman, J. Knox Jones, Jr., and Carleton J. Phillips. REFERENCES Binney, E. C. 1970. Systematics of three species of woodrats (genus Neotoma) in central North America. Ph.D. dissertation, The University of Kansas, Lawrence. Boise, B. P., JR. AND P. N. MouttHrop. 1942. The Ohio Recent mammal collection in the Cleveland Museum of Natural History. Sci. Publ. Cleveland Mus. Nat. Hist., 5:83-181. CuHoaTE, J. R. 1968. Dental abnormalities in the short-tailed shrew, Blarina brevicauda. J. Mamm., 49:251-258. Cuoate, J. R. 1970. Systematics and zoogeog- raphy of Middle American shrews of the genus Cryptotis. Univ. Kansas Publ., Mus. Nat. Hist., 19:195-317. Cuoate, J. R. 1972. Variation within and among Connecticut populations of the short-tailed shrew. J. Mamm., 53:116-128. Cuoate, J. R., anD H. H. GENoways. 1967. Notes on some mammals from Nebraska. Trans. Kan- sas Acad. Sci., 69:238-241. Dice, L. R. 1931. The occurrence of two sub- species of the same species in the same area. J. Mamm., 12:210-213. FINDLEY, J. S. 1955. Speciation of the wandering shrew. Univ. Kansas Publ., Mus. Nat. Hist., 9:1-68. Genoways, H. H., Aanp J. R. CuHoate. 1970. Additional notes on some mammals from eastern Nebraska. Trans. Kansas Acad. Sci., 73:120—-122. Guitpay, J. E., P. S. Martin, anp A. D. Mc- Crapy. 1964. New Paris No. 4: A Pleistocene cave deposit in Bedford County, Pennsylvania. Bull. Natl. Speleol. Soc., 26:121-194. Haut, E. R., anp K. R. Ketson. 1959. The mammals of North America. Ronald Press, New York, 1:xxx-++1-546-+-79. Harris, V. T. 1954. Experimental evidence of reproductive isolation between two subspecies of Peromyscus maniculatus. Contrib. Lab. Vert. Biol., Univ. Michigan, 70:1-13. Hisparp, C. W. 1970. Pleistocene mammalian local faunas from the Great Plains lowland provinces of the United States. Pp. 395-433, in Pleistocene and Recent environments of the central Great Plains (W. Dort, Jr., and J. K. Jones, Jr., eds.), Spec. Publ. 3, Dept. Geol., Univ. Kansas, xii+433 pp. HorrMann, R. S., AND J. K. Jones, Jr. 1970. Influence of late-glacial and post-glacial events on the distribution of Recent mammals on the northern Great Plains. Pp. 356-394, in Pleisto- cene and Recent environments of the central Great Plains (W. Dort, Jr., and J. K. Jones, Jr., eds.), Spec. Publ. 3, Dept. Geol., Univ. Kansas, xii+433 pp. Hooper, E. T. 1942. An effect on the Peromyscus maniculatus rassenkreis of land utilization in Michigan. J. Mamm., 23:193-196. 102 116 SYSTEMATIC ZOOLOGY Joticorur, P. 1959. Multivariate geographical variation in the wolf Canis lupus L. Evolution, 13:283-299. Jones, J. K., Jr. 1964. Distribution and taxonomy of mammals of Nebraska. Univ. Kansas Publ., Mus. Nat. Hist., 16:1—356. Jones, J. K., Jn., AND J. S. FinpLEy. 1954. Geo- graphic distribution of the short-tailed shrew, Blarina brevicauda, in the Great Plains. Trans. Kansas Acad. Sci., 57:208-211. Jones, J. K., Jn., AND B. P. Grass. 1960. The short-tailed shrew, Blarina brevicauda, in Okla- homa. Southwestern Nat., 5:136—142. Key, K. H. L. 1968. The concept of stasipatric speciation. Syst. Zool., 17: 14-22. Kinc, J. A. 1948. Maternal behavior and be- havioral development in two subspecies of Peromyscus maniculatus. J. Mamm., 39:177— 190. LAWRENCE, B., AND W. H. Bossert. 1969. The cranial evidence for hybridization in New En- gland Canis. Breviora, Mus. Comp. Zool., 330: 1-13. Ler, M. R., ann E. G. ZIMMERMAN. 1969. Robertsonian polymorphism in the cotton rat, Sigmodon fulviventer. J. Mamm., 50:333-339. Lone, C. A. 1965. The mammals of Wyoming. Univ. Kansas Publ., Mus. Nat. Hist., 14:493- 758. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, xiv-+-797 pp. MerriAM, C. H. 1895. Revision of the shrews of the American genera Blarina and Notiosorex. N. Amer. Fauna, 10:5-34, 102-107. 103 Meyuan, A. 1967. Formules chromosomique et polymorphisme Robertsonian chez Blarina brevi- cauda (Say) (Mammalia: Insectivora). Cana- dian J. Zool., 45:1119-1127. Oescu, R. D. 1967. A preliminary investigation of a Pleistocene vertebrate fauna from Crank- shaft Pit, Jefferson County, Missouri. Bull. Natl. Speleol. Soc., 29:163-185. PARMALEE, P. W. 1967. A Recent cave bone deposit in southwestern Illinois. Bull. Natl. Speleol. Soc., 29:119-147. Risinc, J. D. 1968. A multivariate assessment of interbreeding between the chickadees, Parus atricapillus and P. carolinensis. Syst. Zool., 17: 160-169. Risinc, J. D. 1970. Morphological variation and evolution in some North American orioles. Syst. Zool., 19:315-351. SCHNELL, G. D. 1970. A phenetic study of the suborder Lari (Aves) I. Methods and results of principal components analyses. Syst. Zool., 19:35-57. Smiru, H. M. 1965. More evolutionary terms. Syst. Zool., 14:57-58. VAUGHAN, T. A. 1967. Two parapatric species of pocket gophers. Evolution, 21:148-158. Wuirtr, M. J. D. 1968. Models of speciation. Science, 159:1065-—1070. Waite, M. J. D., R. E. Bhackwitn, R. M. BLAcK- WITH, AND J. CHENEY. 1967. Cytogenetics of the viatica group of morabine grasshoppers. I. The “coastal” species. Australian J. Zool., 15: 263-302. (Received March 10, 1971) SECTION 2—ANATOMY AND PHYSIOLOGY Form and function are intimately related. It is difficult to consider one at all thoroughly without considering the other. In taxonomy, classification begins with individuals and proceeds through local aggregates or populations, geographic variants, subspecies, and species, and on to groupings at the level of higher categories. In ecology, the individual organism is the basic unit, and progressively more inclusive and more complex levels are local species populations, local communities and ecosystems of many species, and finally the entire biosphere of life-supporting parts of the surface of the Earth. Similarly, in anatomy and physiology there are organizational levels. However, in these fields the individual is the largest unit instead of the smallest, except as we may speak of the anatomical characters of a species or other taxon. Form or function may be studied at the biochemical or molecular level, or at progressively higher levels through more complex molecules, or- ganelles, cells, tissues, organs, systems, and finally to the organism in its entirety. The study of anatomy began at the gross level and only after the invention of the microscope and development of special techniques of preparing ma- terials did histological and cytological studies become possible. Physiology developed later than gross anatomy and in many ways paralleled chemistry and physics. Our selection of examples is a modest one, drawn from a rich field, and while none has electron photomicrographs or histochemical analyses, they do, nevertheless, serve to illustrate some fundamental biological concepts. The concept of homeostasis was conceived and broadly applied in physi- ology. We judge that homeostasis or the tendency of an organism to maintain internal conditions at a dynamic equilibrium is the most general concept of physiology, and that homology is the most general concept of anatomy. This concept is implicit in every comparative study of anatomy, and hence in some of the papers reproduced here. For an explicit treatment of the concept see Bock (1969). Most anatomical and physiological studies are not comparative, and deal with one species only, focusing on the description or mechanisms of form and function. The contributions by Hooper and Hughes are comparative studies within one family (Cricetidae) and one order (Marsupialia), respectively. Each author studied a different part of the animals concerned, in this case reproductive structures, and attempted to relate his observations to existing knowledge within the systematic framework. Many comparative studies deal with other organ systems. Techniques are also extremely important. Just as the light microscope opened new vistas for anatomy of cells and tissues, so the recent development of electron microscopy and the scanning electron microscope have greatly in- creased magnifications. The use of radioisotopes is another important recent development in technique. The next paper, by Noback, treats hair, one of the unique features of the Class Mammalia, and theorizes about its adaptive and phylogenetic implica- 105 tions. This article is from a symposium that contains other interesting papers on hair. The three reprinted papers of Hildebrand, Evans and Maderson, and Rabb treat form and function together, of entire animals during high speed locomo- tion, of part of the respiratory system as it relates to vocalization, and of the poisonous salivary glands of one species, respectively. Among the classic works in mammalian anatomy is Weber's Die Sdugetiere (1927, 1928). English mammalogists dating back to Richard Owen and earlier have published many comparative papers on mammalian anatomy (see for example Pocock’s The External Characters of the Pangolins, 1924). One of the most productive American mammalian anatomists was A. B. Howell, whose Anatomy of the Wood Rat (1926) and Aquatic Mammals (1930) both have much to offer. Four good recent works of a comparative nature are Rinker’s (1954) study of four cricetine genera, Vaughan’s (1966) paper on flight of bats, Klingener’s (1964) treatment of dipodoid rodents, and D. Dwight Davis’ major work (1964) on the giant panda. The ANAToMIcAL REcorp and JOURNAL oF MorruHo.ocy are two of the more important serial publications containing papers on anatomy. Among the environmental influences that are important to organisms, and the effects of which within the organism must be mitigated, are water, oxygen and other gases, energy sources (food), ions, temperature, and radiation. Most of these factors are touched upon in one or more of the last three papers in this selection in ways that help clarify the adaptive nature of internal, be- havioral, and ecological responses. In addition to these aspects of physiology, some areas of special mammalogical interest are hibernation (Kayser, 1961), estivation, thermoregulation, and sensory physiology. A paper by Brown (1968), too long to include among our selections, is an excellent example of how physiological adaptations, related in this case to environmental temperature, can be studied comparatively. Other important contributions in mammalian physiology can be found in such journals as CoMPARATIVE BIOCHEMISTRY AND PHysIOLOGY, JOURNAL OF APPLIED PHYSIOLOGY, JOURNAL OF CELL AND COMPARATIVE PuysIOLocy, and PHysIOLOGICAL ZOOLOGY. 106 NuMBER 625 May 10, 1962 OCCASIONAL PAPERS OF THE MUSEUM OF ZOOLOGY UNIVERSITY OF MICHIGAN ANN ARBOR, MICHIGAN THE GLANS PENIS IN SIGMODON, SIGMOMYS, AND REITHRODON (RODENTIA, CRICETINAE) By EMMET T. HOOPER Corron rats (Sigmodon and Sigmomys), marsh rats, (Holochilus), coney rats (Reithrodon), and red-nosed rats (Neotomys) compose an assemblage which Hershkovitz (1955) considers to be natural and which he designates as the “sigmodont group.” This group contrasts with oryzomyine, ichthyomyine, phyllotine, akodont, and other supraspecific assemblages which various authors (e.g., Thomas, 1917; Gyldenstolpe, 1932; Hershkovitz, 1944, 1948, 1955, 1960; and Voront- sov, 1959) have recognized in analyzing the large cricetine fauna of South America. While all of these groups are tentative, at least in regard to total complement of species in each, nevertheless some are strongly characterized and probably natural; and all, whether natural or not, are useful in that they constitute conveniently assessable seg- ments of an unwieldly large South American cricetine fauna, now disposed in approximately 40 nominal genera. New information re- garding three of those genera is provided below. It is derived from fluid-preserved and partially cleared glandes (procedures described by Hooper, 1959) as follows: Reithrodon cuniculoides: Argentina, Tierra del Fuego, 1 adult. Sigmodon alleni: Michoacan, Dos Aguas, 3 adults. S. hispidus: Arizona, Pima Co., 1 subadult. Florida, Alachua and Osceola coun- ties, 3 adults. Michoacan, Lombardia, 2 adults. S. minimus: New Mexico, Hidalgo Co., 1 juvenile. S. ochrognathus: Texas, Brewster Co., 1 subadult. Sigmomys alstoni: Venezuela, Aragua, 1 subadult. I am indebted to Elio Massoia for the specimen of Reithrodon and to Charles O. Handley, Jr., for the example of Sigmomys. Figures | and 2 were rendered by Suzanne Runyan, staff artist of the Museum of Zoology. The National Science Foundation provided financial aid. Listed below in sequence are representative measurements (in mm.) 107 2 Emmet T. Hooper Occ. Papers of Sigmodon hispidus (averages of five adults), Sigmomys alstoni (one subadult), and Reithrodon cuniculoides (one adult). Length of hind foot: 34, 30, 33; greatest lengths of glans, 7.6, 6.6, 7.8; greatest diam- eter of glans, 6.2, 4.0, 5.0; length of main bone of baculum, 5.5, 4.9, 4.1: length of medial distal segment of baculum, 2.8, 2.0, 2.7; total length of baculum, 8.3, 6.9, 6.8. DESCRIPTION OF GLANDES Sigmodon hispidus.—In Sigmodon hispidus the glans is a spinous, stubby, contorted cylinder (Fig. 1), its length one-fourth to one-fifth that of the hind foot and its greatest diameter approximately three- fourths its length (see measurements). The spines which densely stud almost all of the epidermis, except that of the terminal crater, are short and thick-set; each is recessed in a rhombic or hexagonal pit. The glans is somewhat swayback and potbellied, yet in its basal one-half or two-thirds it is essentially plain and cylindrical, without lobes or folds other than a short midventral frenum which, as an indistinct raphe, continues distad to the rim of the crater. The distal third or half of the glans is conspicuously hexalobate, the six lobes separated from each other by longitudinal troughs or grooves which increase in depth distad. The lobes are unequal in size and shape; the ventral pair is largest and the least convex, the lateral pair smallest, and the dorsal pair the most convex; the latter is a key item in the swayback appearance of the glans. These lobes converge distally, and their crescentic lips form the scalloped, overhanging rim of the terminal crater. The largest structure in the crater is the mound which houses the medial distal segment of the baculum. Nestled between the lips of the ventral lobes, it projects outside the crater approximately to the limits of the dorsal lobes. The two smaller lateral mounds, housing the lateral processes of the baculum, are closely appressed to the medial mound, and the tip of each is distinctly pointed, rather than gently rounded like the medial mound. Immediately ventral to the medial mound is the meatus urinarius which is guarded ventrally by a ure- thral process. This process consists of a pair of rather thick arms each of which is out-curved and tapers to an obtuse tip (Fig. 1); in one specimen the ventral face of the process is studded with spines. Dorsal to the medial mound is the dorsal papilla, which is a single distensible cone of soft tissue dotted with spines both dorsally and laterally. Two additional pairs of crater conules, here termed “dorsolateral and lateral papillae,” are particularly noteworthy because, insofar as known 108 Glans Penis in Sigmodont Rodents No. 625 | foot glans bac. bone 327 3445 slg eas. i It , incised c epidermal spines, enlarged; e, urethral process, ’ Fic. 1. Views of glans penis of Sigmodon hispidus: a, dorsal; b, lateral; midventrally exposing urethra; d, enlarged, ventral aspect; UMMZ 97270, Florida. 109 4 Emmet T. Hooper Occ. Papers in the New World cricetids studied to date, they are peculiar to Sigmodon and Sigmomys. All four of these are spine-studded, stubby, and smoothly rounded terminally. Each dorsolateral papilla is situated just below the crater rim at the junction of the dorsal and lateral lobes. Each lateral papilla is partly recessed in a pocket on the lower flank of the crater wall alongside a lateral bacular mound. There is no ventral shield (a large mass of tissue between the urethral process and the ventral lip of the crater) as seen in most microtines, and the bacular mounds are relatively free within the crater, there being no partitions connecting the lateral mounds with the crater walls; the urethra empties onto the crater floor, not into a partition-encircled secondary crater within the larger crater, an arrangement seen in some rodent species. Below the crater floor is a right and left pair of bilobed sacs (Fig. 1). each ovoid ventral lobe about 1.5 mm. in length, and each atten- uate dorsal lobe approximately a millimeter longer, its tip extending distad almost to the limits of the main bone of the baculum. These sacs or sinuses emerge from tissues situated beside the corpora cavernosa penis and they extend alongside the baculum and the corpus cavernosum urethra, but they apparently are not parts of either of those structures. Composed entirely of soft tissues and engorged with blood in some specimens, they appear to be continuous with the deep dorsal vein and, thus, they seem to be part of the vascular system. Similar sacs, as illustrated in Phyllotis by Pearson (1958:424) for ex- ample, occur in all of those New World cricetids studied to date that have a four-part baculum; they have not been observed in Peromyscus, Neotoma, or other cricetid groups which are characterized by a simple baculum and glans. The four-part baculum is at least as long as the glans and is one- fourth the hind foot in length (see measurements). The main bone, one-sixth the length of the hind foot, is angular and gross. The dorsal face of its wide and angular base is deeply concave between prominent lateral and proximal condyles to which the corpora cavernosa attach, while the ventral surface is almost flat except for a midventral keel of either cartilage or bone which, spanning approximately four-fifths the length of the bone, terminates at the cartilage of the digital junction. The shaft is oval in cross-section, the dorsoventral diameter exceeding the transverse one; as viewed laterally it is slightly bent and is con- stricted terminally, while in ventral view it is gently tapered distad before expanding to form a distinct terminal head. The three distal segments of the baculum are subequal in length, 110 No. 625 Glans Penis in Sigmodont Rodents 5 the lateral pair slightly shorter than the medial one. They differ con- siderably in shape and amount of ossification. In one breeding adult they are entirely cartilaginous, while in four other adults they con- tain various amounts of osseous tissue in addition to cartilage; proba- bly in very old animals they are entirely osseous. The medial segment, attached to the ventral sector of the main bone, projects distad and slightly ventrad, then it bends abruptly dorsad before terminating in a rounded tip. It is approximately oval in cross section in its distal three-fourths, but in its proximal fourth it is much wider than deep and is keeled ventrally; moreover, at the digital junction it bears a pair of lateral processes and a medial flange, the continuation of the midventral keel, which extends over the ventral face of the head of the main bone. In all specimens at hand these three processes are cartilaginous; furthermore, the osseous tissue of the three distal seg- ments is restricted to, or concentrated in, the distal parts of each seg- ment, indicating that ossification apparently proceeds from the tip proximad in S. hispidus. The lateral segments, situated dorsolateral to the medial unit, attach onto the dorsal and lateral parts of the head of the main bone— dorsal to the flanges of the medial segment. Each is pointed and blade- shaped, the dorsoventral diameter exceeding the transverse one; and as viewed ventrally each curves gently distad and slightly laterad. Whether cartilaginous or osseous, they are situated in the lateral parts of each bacular mound, while the medial and distalmost parts of each mound consist entirely of soft tissue, a large part of which is vascular and appears to be instrumental in distention of the mounds. In some examples, the basal parts of the three distal segments of the baculum are more or less coalesced; this is particularly true of the two lateral units, and the two have been interpreted as a single horn-shaped structure (Hamilton, 1946). However, as indicated by Burt (1960) they are separate units (Fig. 1); their individual limits are clear in speci- mens at hand. Sigmodon minimus, S. ochrognathus, and S. alleni.—I recognize no interspecific differences in the specimens of minimus and ochrognathus, both examples of which are young and rather unsatisfactory. Each closely resembles specimens of hispidus of like age in external size and shape, and in conformation of the six exterior lobes, dorsal papilla, dorsolateral papillae, lateral papillae, urethral process, crater mounds, and baculum. If there are interspecific differences, they are not clearly evident in the materal at hand. The three adults from Dos Aguas, Michoacan, which are labeled S. itt 6 Emmet T. Hooper Occ. Papers alleni, are also like adults of hispidus. The two series differ slightly in regard to size of glans and shape of baculum, but these are small differences and doubtfully interspecific. A few remarks regarding the identification of the specimens from Dos Aguas are needed. Until variation in Sigmodon is better under- stood, S. alleni seems to be the most appropriate name to apply to these specimens and, as well, to others like them from the vicinity of Autlan, Jalisco, and Angahuan and Uruapan, Michoacan. Cranially and externally distinguishable from specimens of S. hispidus and S. melanotis from nearby localities in the same states, they appear to represent a species other than either hispidus or melanotis. They agree well with the description of alleni, but they have not been com- pared directly with the type specimen of that form. Sigmomys alstoni.—The specimen of Sigmomys alstoni resembles examples of Sigmodon of comparable age in length (relative to hind foot), in external configuration (hexalobate, swaybacked and _pot- bellied in lateral view, and covered with proximally directed, thickset, sharp, entrenched spines), shape of dorsal papilla (single, spine-stud- ded cone), appearance of urethral process (two outcurved arms with a longitudinal row of spines on the ventral face of each), shape of the bacular mounds (the medial one large and rounded, each lateral one smaller and rounded laterally but acute medially), position of digits of baculum with respect to the main bone, presence of ventral keel and lateral arms on the medial digit, and occurrence of a midventral keel on the main bone. The specimen differs from examples of Sigmodon in characters as follows: glans smaller in diameter (diam- eter-length ratio approximately 60 per cent, compared with 70-88 per cent in Sigmodon); the six external lobes, particularly the dorsal pair, less prominent; dorsolateral papillae smaller, scarcely more than the spine-studded infolding of the dorsal and lateral lobes; crater more extensively spinous (spines studding most of inner wall of each lateral lobe); medial digit of baculum projecting principally distad, its tip not sharply flexed dorsad; and the osseous proximal segment flatter and wider for a larger fraction of its length. The lateral papillae and baculum warrant additional comment. It is uncertain whether lateral papillae are present in the specimen. Two papillose vascular cores occur at sites where papillae are to be ex- pected, but in the present damaged specimen the overlying crater floor is not correspondingly papillose, although it is strongly spinous; the spiny area occupies most of the inner face of the lateral lobe and of the adjoining crater floor. On the left side of the specimen this 112 No. 625 Glans Penis in Sigmodont Rodents 7 roughly circular spiny area is plate-like, while on the right side it is buckled distad and, thus, resembles a large papilla. If, in undamaged specimens, these areas are papillose, then the lateral papillae in S. alstont are relatively larger than any yet seen in Sigmodon. In ventral view, the main bone of the baculum is shaped roughly like an isosceles triangle—wide basally and tapered rather evenly dis- tad (without pronounced incurve) almost to the slight constriction which subtends the small, round, terminal head. Its wide basal part is concave dorsally (between low lateral condyles) and almost flat ventrally; but farther distad the bone is deeper than wide and, some- what triangular in cross section, it bears a slight midventral ridge to which a cartilaginous keel is attached. The distal segments are entirely cartilaginous. The medial one is deeper than wide in its distal half and blunt terminally; basally it bears a medial process and two lateral flanges. Each lateral segment, also deeper than wide and blunt termin- ally, is situated dorsolateral to the medial unit. Reithrodon cuniculoides—The glans of R. cuniculoides (Fig. 2) is stubby (diameter-length ratio 64 per cent), subcylindrical, and indis- tinctly lobate, the lobes defined by four, shallow, longitudinal troughs. Two of these depressions, one situated middorsally and the other midventrally, extend approximately the full length of the glans and thereby divide the surface of the glans into right and left halves; the distal limit of each is a notch in the crater rim. The shorter third pair of troughs is situated dorsolaterally in the distal half of the glans, but each terminates short of the rim. All of the epidermis as far distad as the crenate, membranous, overhanging rim of the crater is densely studded with small, conical, recessed tubercles. The three bacular mounds, together with the underlying baculum, resemble a fleur-de-lis in ventral aspect (Fig. 2); the erect medial part extends beyond the crater, while each of the truncate lateral pair sends off an attenuate lateral segment which curves laterad and then distad before terminating in an acute tip. These lateral processes con- tain no cartilage or bone; they consist entirely of soft tissues, a large part of which is vascular and apparently erectile. The spine-tipped dorsal papilla is unusually small and slender; it is a single cone, but a slight cleft near its tip suggests that the papilla may consist of two conules in other specimens. The urethral process is a bilobed flap with two attenuate and erect (not outcurved) arms; it bears two longi- tudinal rows, each of eight tubercles, on its ventral face. There are no lateral or dorsolateral papillae, and the crater walls and floor are smooth and non-spinous. 113 I I Occ. Papers foot glans bac. bone Seville Miia ie ihesees= Stee SOT ue Aa eX i : AN CR “s wen eS fo 7B SAY Emmet T. Hooper rte? COATT AY POMPOM Fic. 2. Views of glans penis of Reithrodon cuniculoides; UMMZ 109233, Argen- 114 tina. For explanation see Fig. 1 and text. No. 625 Glans Penis in Sigmodont Rodents 9 The baculum is shorter than the glans (see measurements). Its prox- imal, osseous segment consists of a wide basal part and a slender shaft. The basal part, which bears large, proximally directed condyles (these separated medially by a deep notch), is broadly concave ventrally and narrowly and shallowly concave dorsally. The relatively straight shaft is slightly deeper (dorsoventrally) than wide and it bears a slight ventral keel; its terminal portion is slightly expanded laterad and slightly constricted dorsoventrally (Fig. 2). The three distal segments are cartilaginous. The long medial one (its length two-thirds that of the bone) is rod-like for much of its length, but it is enlarged basally and is tapered distally to a pointed tip. The lateral units are disc- shaped in cross section, the dorsoventral diameter of each much great- er than the transverse one. From its attachment on the head of the bone (the attachment dorsal and lateral to that of the medial unit) each lateral segment curves gently laterad and distad before it termin- ates at the base of the laterally projecting process of its lateral mound. DISCUSSION To judge from specimens at hand, the glandes of Sigmodon alleni, S. hispidus, S. minimus, and S. ochrognathus are fundamentally alike, although they may differ interspecifically in details which can not be appraised in present samples. In each species the stubby, swayback, tubercle-invested glans bears six prominent exterior lobes which sur- round the terminal crater and divide its rim into six corresponding parts. Within the crater there are five spine-studded papillae consist- ing of dorsolateral and lateral pairs in addition to a single cone mid- dorsally. ‘The urethral process bears two attenuate, outcurved arms. The bacular mounds are truncate except for a small, acute medial crest on each lateral mound, and the medial distal segment of the four-part baculum bears a medial keel and a pair of lateral processes on its base, while its tip is flexed sharply dorsad. These characters, together with others, distinguish Sigmodon from the other New World cricetid genera which have been studied to date, with the possible exception of Sigmomys. Sigmomys alstoni, the only species of Sig- momys about which there is information on the glans, appears to be closely similar to species of Sigmodon, but its characters are not yet adequately known. In contrast to the phalli of Sigmodon and Sigmomys, the glans of Reithrodon cuniculoides is comparatively slim and simple. There are only four exterior lobes, and these are less prominent than the lobes of Sigmodon or Sigmomys. ‘The membranous, crenate, and non-spiny 115 10 Emmet T. Hooper Occ. Papers crater rim is not divided into six distinct lobes. The crater, also smooth and spineless, has no dorsolateral or lateral papillae. The slender dorsal papilla bears spines only at its tip. Each lateral mound has an attenuate lateral process, and the entire configuration of the three crater mounds as well as of the underlying baculum is distinc- tive. The three, long, erect distal segments of the baculum, all car- tilaginous insofar as known, are essentially rod-like in form, without prominent keels or processes. These and other contrasting characters indicate that the glans of R. cuniculoides is morphologically quite different from that seen in Sigmodon and Sigmomys. Preliminary comparisons suggest that it may be more similar to glandes of phyllo- tine or other species which are not now included in the sigmodont group of rodents. 116 No. 625 Glans Penis in Sigmodont Rodents i | LITERATURE CITED Burt, WILLIAM H. 1960 Bacula of North American mammals. Miscl. Publ. Mus. Zool. Univ. Mich., 113:1-76, 25 pls: GYLDENSTOLPE, NILS 1932. A manual of Neotropical sigmodont rodents. Kungl. Svenska Veten. Hand., Ser. 3, no. 3: 1-164, 18 pls. HAMILTON, WILLIAM J., JR. 1946 A study of the baculum in some North American Microtinae. Jour. Mamm., 27:378-87, 1 pl., 3 figs. HERSHKOVITZ, PHILIP 1944 A systematic review of the neotropical water rats of the genus Nectomys (Cricetinae). Miscl. Publ. Mus. Zool. Univ. Mich., 58:1-88, 4 pls., 5 figs. 1948 Mammals of northern Colombia, preliminary report No, 3: water rats (genus Nectomys), with supplemental notes on related forms. Proc. U.S. Natl. Mus., 98:49-56, 1955 South American marsh rats, genus Holochilus, with a summary of sig- modont rodents. Fieldiana: Zoology, 37:639-73, 13 pls., 6 figs. 1960 Mammals of northern Colombia, preliminary report No. 8: arboreal rice rats, a systematic revision of the subgenus Oecomys, genus Oryzomys. Proc. U.S. Natl. Mus., 110:513-68, 12 pls., 6 figs. Hooper, EMMET T. 1959 The glans penis in five genera of cricetid rodents. Occ. Pap. Mus. Zool. Univ. Mich., 613:1-10, 5 pls. PEARSON, OLIVER P. 1958 A taxonomic revision of the rodent genus Phyllotis. Univ. Calif. Publ. Zool., 56:391-496, 8 pls., 21 figs. THOMAS, OLDFIELD 1917 On the arrangement of the South American rats allied to Oryzomys and Rhipidomys. Ann. Mag. Nat. Hist., ser. 8, 20:192-8. Vorontsov, N. N. 1959 The system of hamster (Cricetinae) in the sphere of the world fauna and their phylogenetic relations. Bull. Mosk. Obsh. Ispyt. Prirody, Biol. Sec. (Bull. Moscow Soc. Naturalists), 64:134-7. Accepted for publication February 5, 1962 117 COMPARATIVE MORPHOLOGY OF SPERMATOZOA FROM FIVE MARSUPIAL FAMILIES By R. L. HUGHES* [Manuscript received April 8, 1965] Summary The spermatozoa of 18 marsupial species derived from five families have been examined and of these only the spermatozoon of the bandicoot Perameles nasuta has previously been described adequately. The spermatozoon morphology within the families Macropodidae, Dasyuridae, Phascolarctidae, and Peramelidae was relatively homogeneous. A _ distinctive morphology occured between these families. Within the family Phalangeridae spermatozoa were morphologically diverse, however, as a group they were relatively separate from those of the other families studied. The spermatozoa of the Phascolarctidae (koala, Phascolarctos cinereus, and wombat, Phascolomis mitchelli) have a unique, somewhat rat-like morphology which clearly separates them from those of the other marsupial sperm studied. This finding is of considerable taxonomic interest as most authorities consider the koala to be more closely related to the phalangerid marsupials than to the wombat. I. INTRODUCTION Previous descriptions of marsupial spermatozoon morphology cover six of the major marsupial groups. A considerable proportion of these accounts is devoted to a study of the spermatozoon morphology of three species, each belonging to separate marsupial families. (1) Family Didelphidae: Didelphis [Selenka (1887), Furst (1887), Waldeyer (1902), Korff (1902), Retzius (1909), Jordan (1911), Duesberg (1920), Wilson (1928), McCrady (1938), Biggers and Creed (1962)]; (2) family Phalangeridae: Phalangista vulpina ( = Trichosurus vulpecula) [Korff (1902), Benda (1897, 1906), Retzius (1906), Bishop and Walton (1960)]; (3) family Peramelidae: Perameles nasuta [Benda (1906), Cleland (1955, 1956, 1964), Cleland and Rothschild (1959), Bishop and Austin (1957), Bishop and Walton (1960)]. The spermatozoon morphology of two Dasyuridae, Phascogale albipes ( = Smin- thopsis murina) and Dasyurops maculatus, was studied by First (1887), Bishop and Austin (1957), and Bishop and Walton (1960). Benda’s (1906) description of an epididymal sperm from the koala, Phascolarctos (family Phascolarctidae), is, as he admits, inadequate. Spermatozoon morphology studies on members of the family Macropodidae include those of an unknown Macropus sp. (Benda 1906), Macropus billardierii ( = Thylogale billardierii), Petrogale penicillata, Onychogale lunata ( = Onychogalea lunata), Bettongia cuniculus (Retzius 1906), Macropus giganteus ( = Macropus canguru) (Binder 1927), and Potorous tridactylus (Hughes 1964). * Division of Wildlife Research, CSIRO, Canberra. Aust. J. Zool., 1965, 13, 533-43 118 534 R. L. HUGHES The spermatozoa examined in the present study were obtained from members of the five Australasian marsupial families: Phalangeridae, Peramelidae, Dasyuridae, Phascolarctidae, and Macropodidae. The present series of observations has been viewed with reference to those of earlier workers and this has permitted at least an elementary discussion of the comparative aspects of spermatozoon morphology between the marsupial families examined. Il. MATERIAL AND METHODS The testes together with the attached epididymis were removed from the scrotum soon after death and fixed in 10% neutral formalin or, more rarely, Bouin’s fluid or Carnoy fixative. (i) Method for Adhering Spermatozoa to Microscope Slides The slides were labelled at one end with a diamond pencil and a 15-mm square was marked out at the opposite end. The entire surface of the slide was liberally smeared with Mayer’s albumen. A small piece of epididymal tissue was placed in a drop of 10% neutral buffered formalin within the marked square and extensively teased with dissecting needles. Filter paper circles of 5-5 cm diam. were saturated with 10% formalin, drained, and placed over the specimen by a rolling action. Air bubbles were punctured with a needle. The filter paper was kept moist with 10% formalin for at least 30 min and then permitted to dry until free fluid between the slide and the filter paper had disappeared. The filter paper was then removed by a rolling action, excess tissue was removed with fine forceps, and the preparations rinsed and stored in water for staining. (11) Staining of Spermatozoa (1) Heidenhain’s Iron Haematoxylin.—Slides containing adhering spermatozoa were transferred from water to a 5% solution of iron alum and kept in a warm place for 2-3 days. They were then stained with Heidenhain’s haematoxylin for a similar period. The area not containing the specimen was thoroughly cleaned with paper tissues during a 10-15 min rinsing period in running tap water. The preparations were then differentiated in 5% iron alum under a staining microscope at 30 sec intervals. The preparation was washed in water and re-examined after each differentiation inter- val. Differentiation times of between 30 sec and 5 min proved satisfactory to show the desired range of structures. The preparations were upgraded to absolute ethyl alcohol, placed in two changes of xylol, and mounted in euparal. (2) Periodic Acid—Schiff (with saliva controls).—Slides containing the mounted spermatozoa were removed from water and placed horizontally in two groups on a flat tray. One group was flooded with water and the other with saliva for | hr at a temperature of 37°C. The slides were then thoroughly rinsed in distilled water and stained by a method described by Carleton and Drury (1957, p. 143). The Schiff’s reagent used was de Tomasi (for preparation see Pearse 1961, p. 822). The prepara- tions were mounted in euparal. (3) Feulgen (with and without fast green counterstain).—Slides containing the adhering spermatozoa were removed from water and stained by a method described 119 MORPHOLOGY OF SPERMATOZOA 535 by Pearse (1961, p. 823). The Schiff’s solution used was de Tomasi. Half the Feulgen preparations were stained with fast green counterstain (0-5% solution in 70% ethyl alcohol) for 15-20 min. Both Feulgen and Feulgen-fast green preparations were quickly passed through three changes of 90% alcohol (dips only) to absolute ethyl alcohol and then cleared in xylol and mounted in euparal. Slides were stored until dry in an oven at a temperature of 37°C after mounting in euparal. Preparations were not permitted to dry out during any of the earlier stages in preparation. The drawings of spermatozoa shown in Figure | are based on camera lucida outlines using a X12 eyepiece in conjunction with a 100 oil-immersion objective. The spermatozoon dimensions shown in Table | are means of 25 observations and were obtained with a special Leitz x 12-5 screw micrometer eyepiece and a x 100 oil-immersion objective. The preparations used were fixed in 10% neutral formalin or, more rarely, Bouin’s fluid or Carnoy and were stained with Heidenhain’s iron haematoxylin. During the course of the observations on sperm it became apparent that the efferent ducts connecting the testis and epididymis were either multiple or single within each marsupial family. This was investigated further from frozen transverse sections stained with haematoxylin and eosin. The sections were prepared from the efferent duct or ducts at the point of their emergence from the testis and also approxim- ately midway between the testis and epididymis. The author follows Cleland and Rothschild (1959) in considering for the purpose of description that the flagellum is inserted into the ventral surface of the sperm head and the opposite surface is taken as dorsal. III. RESULTS The mature epididymal spermatozoa of 18 marsupial species have been examined. The dimensions of 13 of these spermatozoa are shown in Table |. The gross morphol- ogy of 14 of the spermatozoa is shown in Figure 1. Spermatozoa of each of the five marsupial families studied (Macropodidae, Phalangeridae, Dasyuridae, Peramelidae, Phascolarctidae*) exhibited sufficient homogeneity in morphology and dimensions of the head, flagellum, and fine structure to be of taxonomic value. The heads of all marsupial spermatozoa examined showed some dorsoventral flattening. This was most marked in the Dasyuridae and Peramelidae. It was least evident in the Phascolarctidae and the genus Pseudocheirus of the Phalangeridae. Macropod and the other phalangerid spermatozoa exhibited an intermediate con- dition. The distal extremity of the head of all species when viewed dorsally was relatively rounded while the shape of the lateral margins and proximal tip varied considerably. In the Dasyuridae the spermatozoon heads of up to 12-7 » in length in Dasyuroides byrnei are among the longest known for mammals (Table 1). The * The author follows Sonntag (1923) in grouping the wombat and koala in the family Phascolarctidae. 120 536 R. L. HUGHES lateral head margins of dasyurid sperm are slightly convex in dorsal view and taper gradually to a proximal point. Macropod sperm heads are considerably shorter than those of the Dasyuridae and in dorsal outline are elongated ovoids bluntly pointed proximally. The sperm head of the macropod Megaleia rufa (Figs. 1g and 1h) is rapidly tapering, a condition typically found in the Phalangeridae. Phalangerid sperm, when viewed dorsally, exhibit considerable variability in the convexity of the lateral head margins. The proximal region of the head is typically semicircular, although sometimes bluntly pointed as in Pseudocheirus cupreus (Figs. In and lo). TABLE | MARSUPIAL SPERMATOZOON DIMENSIONS Mean +SD (2) Family and Species Head Middle-piece Flagellurn Length Width | Length Diameter Length Macropodidae | | | | Macropus canguru 7:-340-16 | 2:240-11 | 10-740-24 | 1-540-14 | 111-6+ 3-60 Megaleia rufa* 5-1+0-21 | 2:-4+0-09 7-94+0-°25 | 1-44+0-12 | 104-0+ 4-74 Protemnodon rufogrisea 8-5+0-22 | 2:340-18 | 11:74+0:34 1-6+0-14 | 115-44 8-85 Protemnodon agilist 7-140:°38 | 1-8+0:12 | 11:0+0:28 , 1:44+0-13 = — Thylogale stigmatica* 7-24+0:-09 ; 2-240-11 | 10:9+0-22 | 1-5+0-12 | 103-14 4-43 | Dasyuridae | | Dasyuroides byrnei els TORY 2201S) 40474-12267) 3°10 eno) | 242 ee Go77. Sarcophilus harrisii | E1*1+-0*45°) 2°2--0°17 | 34°44-0°84. 2°64-0-13: |. 20774--12-02 Phalangeridae | | Petaurus brevicepst 5:9+0:19 | 2:5+0:18 8-3+0-27 | 1-4+0-11 | 101-3+ 4-96 Pseudocheirus cupreust 5-4+0:-16 | 2:6+0:11 6°2+0:-16 | 1-50-17 | 84:7+ 2-47 Pseudocheirus peregrinus 5-94+0-38 | 3-8+0-18 6:-9+0-21 | 2:140-22 , 106-94 5-31 Phascolarctidae | Phascolomis mitchelli 5:740:33 1-740-09 18:0+1-56 0:9+0-10 | 87:9+ 8-23 | | Peramelidae | | Perameles nasuta 5:7+0°:15 | 3:0+0:13 | 14-040:32 2:04+0°11 | 194-14 5:25 Isoodon macrourus 6:0+0°13 ; 3:3+0-18 | 10°7+0:19 !' 1-8+0-14 | 165:1+ 3-64 * Fixed in Bouin’s fluid; + Carnoy fixative; { from New Guinea. Peramelid spermatozoon heads have concave lateral margins when seen in dorsal view and are relatively square proximally with a median cap. In phascolarctid sperm the proximal portion of the spermatozoon head of both the wombat Phascolomis mitchelli, and the koala, Phascolarctos cinereus, bears a strongly recurved hook. In all sperm, a positive Feulgen reaction for nuclear material (DNA) was given by almost the entire head mass. The DNA-negative areas that took up a fast green counterstain in Feulgen preparations were the acrosome (Fig. 1; AC) and basal granule complex which is located at the proximal tip of the flagellum. The acrosome 121 MORPHOLOGY OF SPERMATOZOA BOL Gig: ‘ 20u Fig. 1.—Marsupial epididymal spermatozoa: the drawings are all at the same scale and are based on camera lucida outlines of formalin-fixed Heidenhain’s iron haematoxylin preparations. A x 12 eyepiece was used in conjunction with a 100 oil-immersion lens. Fam. Phascolarctidae: Phascolomis mitchelli, (a) lateral view; Phascolarctos cinereus, (b) lateral view of spermatozoon head with flagellum outline. Fam. Macropodidae: Protemnodon rufogrisea, (c) ventral view, (d) lateral view; Protemnodon agilis*, (e) lateral view, (f) ventral view; Megaleia rufat, (g) lateral view, (A) ventral view; Macropus canguru, (i) lateral view; Thylogale stigmaticat, (j) lateral view; (A) ventral view. Fam. Dasyurinae: Dasyuroides byrnei, (1) dorsolateral view; Sarcophilius harrisii, (m) ventral view. Fam. Phalangeridae: Pseudocheirus cupreus, (n) dorsal view, (0) lateral view; Pseudocheirus peregrinus, (p) lateral view, (q) dorsal view; Petaurus breviceps, (r) ventral view. Fam. Peramelidae: Jsoodon macrourus, (s) ventral view; Perameles nasuta, (t) ventral view. Key: AC, acrosome; AF, axial filament; CD, cytoplasmic droplet (middle-piece bead); CH, cortical helix of main-piece sheath; MH, mitochondrial helix of middle-piece; NG, neck granule; RC, ring centriole; VG, ventral groove. * Fixed in Carnoy fixative. + Fixed in Bouin’s fluid. 122 538 R. L. HUGHES was also variably positive to periodic acid—Schiff (P.A.S.) between species and the basal granule complex was invariably strongly P.A.S.-positive. Neither acrosome nor basal granule complex exhibited any reduction in P.A.S. activity in saliva controls. A faint tinge of green over the entire head surface in Feulgen—fast green preparations pre- sumably represents a limiting membrane. A “nuclear rarefaction” of vacuole-like appearance results from a minute superficial nuclear indentation. The nuclear rarefaction was most conspicuous in the Dasyuridae and Peramelidae and least evident in the Macropodidae. This structure is located on the mid-median aspect of the ventral nuclear surface of all sperm with the exception of those of the Phascolarctidae, where its occurrence is also ventral and median but distal. In most of the marsupial sperm examined acrosomal material (Fig. 1; AC) was apparently confined to a relatively small surface area of the head. In the Macropodidae the acrosome is relatively small and is a discrete ovoid structure embedded super- ficially in the extreme proximal portion of the dorsal head surface. In some of the Phalangeridae it has a definite structure as in Pseudocheirus (Figs. In-lq) where it occupies all but a marginal annular zone of the dorsal head surface and is rather deeply embedded. In other phalangerids, such as Petaurus breviceps (Fig. 1r), the dorsal head surface in Feulgen-fast green preparations gives a diffuse acrosomal reaction and bears a shallow depression which extends to all but the margins. A similar diffuse acrosomal reaction of at least the proximal half of the dorsal head surface occurred in the Dasyuridae. The proximal dorsal tip of the dasyurid sperm has a concentration of acrosomal material situated in a minute groove. The acrosomal material in the Peramelidae was found in a small distally flanged proximal cap which covered a minute nuclear protuberance. In the Phascolarctidae the acrosome is a small ““comma-shaped”’ structure. The body of the acrosomal ‘‘comma’”’ is embedded superficially in about the middle of the dorsal head surface and the tail of the comma extends throughout the greater portion of the inner curvature of the head hook. In marsupial sperm the ventral surface of the head (by convention that bearing the flagellum) is typically grooved (Fig. 1; VG) or bears a shallow distal notch as in the case of the Phascolarctidae. At the distal extremity of the head the groove is broad and deep so that the head is here relatively broad and has the form of an extremely thin curved plate. The groove becomes shallow and narrow towards its proximal extremity; in the Macropodidae and Phalangeridae it terminates at about the mid- median portion of the ventral head surface. The groove is most extensive in the Peramelidae involving the whole of the ventral aspect of the nucleus, only the proximal acrosomal head cap is excepted. In the Dasyuridae it extends throughout the distal four-fifths of the head. Spermatozoa are immature when they enter the head of the epididymis and were characterized by the orientation of the long axis of the head at 90° to the flagellum which was directed towards the nuclear rarefaction. The ventral surface of the spermatozoon head was supported by a somewhat cone-shaped cytoplasmic droplet (Fig. 1; CD) of characteristic morphology for each species. Phascolarctid sperm from the head region of the epididymis differed from the other marsupial 123 MORPHOLOGY OF SPERMATOZOA 539 species examined in that the flagellum was most frequently observed not to meet the head at right angles and cytoplasmic droplets were small and often absent. On entering the epididymis the head hook of the phascolarctid spermatozoa were only slightly recurved or of an irregular spiral configuration. During the passage of spermatozoa through the epididymis the head hook became simple (without spiral) and more tightly recurved. Maturation of spermatozoa is completed during their passage through the epididymis and is accompanied by shedding of the cytoplasmic droplet and rotation of the long axis of the head parallel to that of the flagellum. The neck of the flagellum of mature epididymal sperm in all species was inserted in the vicinity of the nuclear rarefaction. In the Dasyuridae the neck was inserted rather deeply into the proximal margin of the nuclear rarefaction. In the Peramelidae the proximal tip of the flagellum was also deeply inserted and extended from the proximal margin of the nuclear rarefaction to a point about midway between the anterior rim of the nuclear rarefaction and the most proximal extremity of the nucleus. The flagellum is traversed throughout its entirety by an axial filament (Fig. 3; AF). The size of the flagellum varies from species to species. The smallest flagellum was that of Phascolomis mitchelli with a maximum diameter of 0-9 uw and a minimum length of 87:9 (Table 1). The giant flagella of dasyurid sperm are among the largest known for mammals. Dasyuroides byrnei has a minimum flagellum length of 242-1 » and a maximum flagellum thickness of 3-1 «. In an old museum specimen of the testes of the now possibly extinct dasyurid Thylacinus cynocephalus (Tasmanian wolf or tiger) the flagellum of epididymal sperm in wax sections had a maximum diameter of 3-0 and comparable morphology to that of other dasyurids; the sperm heads, although degenerate, were in the form of a long narrow plate, dorso- ventrally flattened and with the flagellum inserted at about the mid-median ventral aspect. Peramelid sperm flagellae were also relatively large, having a maximum diameter of as much as 2» and a minimum length of up to about 200 u (Table 1). Macropod and phalangerid sperm flagellae were of intermediate dimensions rarely varying from a maximum diameter of 1-5 and a minimum length of a little over 100 pe. The basal granule complex located at the proximal end of the flagellum consists of at least fused proximal and distal components in the Dasyuridae and Peramelidae. The neck region of the flagellum is a slender proximally pointed cone with a smooth contour, and a small neck granule (Fig. 1; NG) is situated at approximately half its length. It was only possible to identify the neck granule with certainty in the Peramelidae, Dasyuridae, and Macropodidae. In the Peramelidae and Dasyuridae it seemed to be a more deeply stained, modified portion of the ground substance of the neck rather than the discrete granule found in the Macropodidae. The sperm of the dasyurids Dasyuroides byrnei, Sarcophilus harrisii, and Thylacinus cynocephalus had a neck length of about 3-5, in comparison with 2-7 for the peramelids Isoodon macrourus and Perameles nasuta. Macropod sperm necks ranged in length from 1-8 in Thylogale stigmatica to 2-6 » in Protemnodon rufogrisea. The neck lengths of the Phalangeridae and Phascolarctidae were somewhat reduced in compari- son to those of other marsupial families. 124 540 R. L. HUGHES The proximal portion of the middle-piece in all species examined tapered gradu- ally to the diameter of the neck and was particularly firmly clasped by the lateral margins of the sperm head in the Peramelidae and Dasyuridae. The remainder of the middle-piece was relatively cylindrical. A mitochondrial helix (Fig. 1; MH) of spiral configuration gave the entire surface of the middle-piece sheath a slightly uneven contour. The mitochondrial helix is a relatively fine structure in the Dasyuridae and Peramelidae, of moderate thickness in the Macropodidae and Phascolarctidae and Petaurus breviceps of the Phalangeridae. It was quite thick and granular with relatively few gyres in the genus Pseudocheirus of the Phalangeridae. The middle- piece is terminated distally by a ring centriole (Fig. 1; RC). The flagellum undergoes an abrupt reduction in diameter on the main-piece side of the ring centriole in both the Pseudocheirus species and to a moderate degree in Petaurus breviceps and the Macropodidae, but not to any appreciable extent in the Dasyuridae, Peramelidae, and Phascolarctidae. The main-piece of the flagellum tapers distally and in twisted specimens appears not to be circular in cross section in Pseudocheirus peregrinus, Peramelidae, Dasyuridae, and Macropodidae. Striations of the sheath of the main piece in all sperm indicate the presence of a fine spiral cortical helix (Fig. |; CH). The tail sheath also gave a strong impression of two lateral thickenings in transverse axis in Macropus canguru, Protemnodon rufogrisea, Pseudocheirus peregrinus, Perameles nasuta, and Isoodon macrourus. The axial filament protruded beyond the terminal portion of the sheath of the main-piece in apparently complete sperm of all species but this cannot be positively taken to represent a true end-piece for in all preparations terminal breakage of the main-piece was prevalent. IV. DISCUSSION Spermatozoa from three other Peramelidae, Perameles gunnii, Isoodon obesulus, and Echymipera rufescens have also been examined superficially and it can be stated that they are comparable in morphology to other peramelid sperm. The spermatozoa of marsupial mice, Antechinus flavipes flavipes, A. f. leucogaster, A. swainsonii, A. stuartii, and Sminthopsis crassicaudata, have a morphology typical of other dasyurids (Woolley, personal communication). This similarity in morphology also extends to two other dasyurids, Phascogale albipes ( = Sminthopsis murina) (First 1887) and Dasyurops maculatus (Bishop and Austin 1957; Bishop and Walton 1960). The spermatozoon morphology of the macropod species examined in the present study varies in only minor details from that of six other macropods previously described by Benda (1906), Retzius (1906), and Hughes (1964). The phenomenon of conjugate spermatozoa (pairing of relatively numerous epididymal spermatozoa) redescribed and reviewed by Biggers and Creed (1962) for the American opossum, Didelphis, has not been observed in any of the sperm pre- parations from Australian marsupials; however, fresh unfixed material has been examined only for Potorous tridactylus (Hughes 1964) and Phascolomis mitchelli. 125 MORPHOLOGY OF SPERMATOZOA 541 Another feature worth mentioning is that the head of the epididymis was not fused with the testis in any marsupial examined, including Thylacinus cynocephalus and Dendrolagus lumholtzi. In the Dasyuridae and Peramelidae a relatively long single efferent duct together with associated blood vessels links the epididymis to one pole of the testis long axis by way of an extensive membrane, the mesorchium. A tract of relatively long multiple efferent ducts serves the same function in the Phalangeridae, Phascolarctidae, and Macropodidae. A ligament was inserted by way of the mesorchium into the opposite pole of the testis. In both the wombat and the koala the morphology of the sperm, particularly the head, differs strikingly from that of any marsupial sperm previously described. In both species the proximal portion of the spermatozoon head bears a strongly recurved hook not described for other marsupial sperm, and the flagellum is inserted into a notch on one side of the distal portion of the head (Plate 1, Fig. 1; and Figs. la and 1b).. These features, although somewhat resembling those of certain murid sperm, are not strictly comparable (Plate 1, Fig. 2) (Friend 1936). The hook in the wombat sperm resembles that of Microtus hirtus, Lemmus lemmus, and several other members of the murid subfamily Microtinae in that the hook contains no supporting “rod”? and its tip like that of Lemmus lemmus is typically extremely reflected so that it lies against the distal portion of the head (Friend 1936). The position of the hook in Phascolomis is not an artefact of fixation for it was observed in living spermatozoa from the epididymis of several specimens. In sperm from the head of the epididymis the curvature of the hook frequently approximated to that of rats and mice. It can be seen from Plate 1, Figure |, and Figures la and 14 that the insertion notch of the flagellum of the wombat and koala sperm is located on the opposite side of the head to the hook, whereas in the hooked types of murid sperm both structures occur on the same side of the head (Plate 1, Fig. 2). A head hook is absent in at least the murine, Micromys minutus and in the microtine Ondatra zibethica (Friend 1936). In Heidenhain’s iron haematoxylin preparations the head length of the wombat sperm measured from the distal extremity to the most proximal point of the curvature of the hook (i.e. excluding the recurved portion of the hook) is about 5-7 » in contrast to 8-0 and 11-7, for mouse and rat, respectively (Friend 1936). Feulgen pre- parations (with or without fast green counterstain) of wombat and koala sperm have shown that nuclear material (DNA) extends to the tip of the hook and occupies all but a small comma-shaped acrosomal portion of the head. Herein lies the greatest departure of wombat sperm from the hooked varieties of murid sperm. In several microtine species the hook is formed entirely from a proximal extension of the nuclear cap (acrosome). In murine sperm a hooked portion of the nucleus bearing a rod extends into the hooked nuclear cap and follows its contour almost to its proximal extremity (Friend 1936). On the basis of skeletal and dental structure most workers consider the koala to be more closely related to the ringtail possums of the genus Pseudocheirus than the wombat (Wood Jones 1924; Simpson 1945). Comparisons of sperm morphology on which selection pressure would presumably be lower than that for external characters of an animal such as skeletal or dental characters, is therefore of considerable interest as a possible basis for taxonomic classification. 126 542 R. L. HUGHES It can be seen from the previous descriptions that the spermatozoon of Pseudo- cheirus peregrinus is not intermediate in structure between the more typical marsupial types (Macropodidae and Dasyuridae) and those of the highly divergent wombat and koala. On the contrary, it deviates in quite a different manner from the typical marsupial patterns. The head is broad (3-8 «) in comparison to its length (5-9 2), the anterior end lacks a hook and is semi-circular in dorsal view (Plate 1, Figs. 3 and 4). Other distinguishing features are the shape and position of the acrosome previously mentioned and a relatively short middle-piece (6:9). The view that the koala is more closely related to the ringtail possum than the wombat is not supported by comparisons of sperm morphology. On the contrary, the findings reported here support the observations of Sonntag (1923) and Troughton (1957) who considered that the koala shares sufficient characters with the wombat for its classification along with the phalangers to be rejected. V. ACKNOWLEDGMENTS The author wishes to express his sincere thanks to Dr. E. H. Hipsley, Director, Institute of Anatomy, Canberra; to J. T. Woods, Queensland Museum; to J. A. Thomson, Zoology Department, University of Melbourne; to Dr. M. E. Griffiths, W. E. Poole, K. Keith, M. G. Ridpath, Division of Wildlife Research, CSIRO, for material; to J. Sangiau and L. S. Hall for technical assistance; to E. Slater for photography; and to Professor K. W. Cleland and Dr. A. W. H. Braden who offered helpful criticism. VI. REFERENCES BENDA, C. (1897).—Neuere Mittheilungen iiber die Histiogenese der Sdugethierspermatozoen. Verh. berl. physiol. Ges. 1897. [In Arch. Anat. Physiol. (Physiol. Abt.) 1897: 406-14.] BENDA, C. (1906).—Die Spermiogenese der Marsupialier. Denkschr. med.-naturw. Ges. Jena 6: 441-58. Biccers, J. D., and CREED, R. F. S. (1962).—Conjugate spermatozoa of the North American opossum. Nature, Lond. 196: 1112-3. BINDER, S. (1927).—Spermatogenese von Macropus giganteus. Z. Zellforsch. 5: 293-346. BisHop, M. W. H., and Austin, C. R. (1957).—Mammalian spermatozoa. Endeavour 16: 137-50. BisHop, M. W. H., and WALTON, A: (1960).—Spermatogenesis and the structure of mammalian spermatozoa. In ‘‘Marshall’s Physiology of Reproduction”. (Ed. A. S. Parkes.) 3rd Ed. Vol. 1, Pt. 2, pp. 1-129. (Longmans, Green and Co.: London.) CARLETON, H., and Drury, R. A. B. (1957).—‘‘Histological Technique.’’ (Oxford University Press.) CLELAND, K. W. (1955).—Structure of bandicoot sperm tail. Aust. J. Sci. 18: 96-7. CLELAND, K. W. (1956).—Acrosome formation in bandicoot spermiogenesis. Nature, Lond. 177: 387-8. CLELAND, K. W. (1964).—History of the centrioles in bandicoot (Perameles) spermiogenesis. J. Anat. 98: 487. CLELAND, K. W., and Lorp ROTHSCHILD (1959).—The bandicoot spermatozoon: an electron microscope study of the tail. Proc. R. Soc. B 150: 24-42. DUuESBERG, J. (1920).—Cytoplasmic structures in the seminal epithelium of the opossum. Carnegie Institute Contributions to Embryology. Vol. 9, pp. 47-84. FRIEND, G. F. (1936).—The sperms of the British Muridae. Quart. J. Micr. Sci. 78: 419-43. Furst, C. M. (1887).—Ueber die Entwicklung der Samenkorperchen bei den Beutelthieren. Arch. mikrosk. Anat. EntwMech. 30: 336-65. Huaues, R. L. (1964).—Sexual development and spermatozoon morphology in the male macropod marsupial Potorous tridactylus (Kerr). Aust. J. Zool. 12: 42-51. 127 MORPHOLOGY OF SPERMATOZOA 543 JoRDAN, H. E. (1911).—The spermatogenesis of the opossum (Didelphis virginiana) with special reference to the accessory chromosome and the chondriosomes. Arch. Zellforsch. 7: 41-86. KoreF, K. von (1902).—Zur Histogenese der Spermien von Phalangista vulpina. Arch. mikrosk. Anat. EntwMech. 60: 233-60. McCrapy, E. (1938).—The embryology of the opossum. Am. Anat. Mem. 16: 1-233. Pearse, A. G. E. (1961).—‘‘Histochemistry.”” (J. & A. Churchill: London.) Rerzius, G. (1906).—Die Spermien der Marsupialier. Biol. Unters. (N. F.) 13: 77-86. Retzius, G. (1909).—Die Spermien von Didelphis. Biol. Unters. (N. F.) 14: 123-6. SELENKA, E. (1887).—Studien iiber Entwickelungsgeschichte der Thiere. Das Opossum (Didelphis virginiana). Wiesbaden 1887, pp. 101-72. Simpson, G. G. (1945).—Principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 85: 1-350. SONNTAG, C. F. (1923).—On the myology and classification of the wombat, koala and phalangers. Proc. Zool. Soc. Lond. 1922: 683-895. TROUGHTON, E. (1957).—‘*Furred Animals of Australia.”’ 6th Ed. (Angus and Robertson: Sydney.) WALDEYER, W. (1902).—Die Geschlechtszellen. In “Handbuch der vergleichend und experimentellen Entwickelungsgeschichte der Wirbelthiere’’. Vol. 1, Pt. 1, pp. 86-476. WILSON, E. B. (1928).—‘The Cell in Development and Heredity.” (Macmillan: New York.) Woop Jones, F. (1924).—**The Mammals of South Australia.” Pt. If. (Govt. Printer: Adelaide.) EXPLANATION OF PLATE | Figures 1 and 2 are photographs of Heidenhain’s iron-haematoxylin preparations from formalin-fixed epididymal material Fig. 1.—Phascolomis mitchelli, mature epididymal spermatozoon, lateral view. Fig. 2.—Rattus norvegicus, mature epididymal spermatozoon, lateral view. Fig. 3.—Pseudocheirus peregrinus, spermatozoon head, showing centrally placed acrosomal pit, dorsal view. Fig. 4.—Pseudocheirus peregrinus, epididymal spermatozoon, lateral view. 128 HUGHES PLATE 1 MORPHOLOGY OF SPERMATOZOA Aust. J. Zool., 1965, 13, 533-43 129 AMER. ZOOL., 13:1205-1213 (1973). Mechanisms of Sound Production in Delphinid Cetaceans: A Review and some Anatomical Considerations WILLIAM E. EVANS Naval Undersea Center, San Diego, California 92132 AND PAUL F. A. MADERSON Department of Biology, Brooklyn College, Brooklyn, New York 11210 synopsis. The past literature describing the possible sites of the sound-producing mechanisms in delphinid cetaceans is reviewed. The morphology of the nasal sac system of delphinids which has been implicated in the production of sounds, ‘by most investigations, is discussed with special emphasis placed on the physical characteris- tics of these sounds. New data on the histological structure of the epithelia through- out the nasal region of a delphinid are presented with some suggestions as to its function. The presence and structure of glandular tissues are described along with a discussion of their potential role in the production of sound. It is concluded that the theories implicating the nasal sac systems of odontocete cetaceans in the produc- tion of sound are additionally supported by certain anatomical specializations ad- jacent to the tissues of this system. All the theories to date concerning the mechanism of delphinid sound production have implicated the larynx (arytenoepiglot- tic tube), the complicated diverticuli asso- ciated with the blowhole mechanism, the large muscular plugs that seal off the in- ternal nares, or various combinations of these. The driving mechanism has been thought to be pneumatic, mechanical (muscle-driven), or both. Various combina- tions of internal sound transmission paths have been considered: air—muscle/fat— water; air—bone—water; tissue—water (Nor- ris, 1969; Evans, 1973). Attempts have been made to construct conceptual models of the delphinid sound source so that the models could be com- pared with existing anatomical structures as an aid in localizing the sound source. Unfortunately most of the current ideas, with the exceptions of Norris and Harvey (1972) and Evans (1973), have not con- sidered the acoustical parameters of the signals being produced by the ‘theoretical’ Maderson’s work is supported in part by grants AM-15515 and CA-10844 from the National Insti- tute of Health and C.U.N.Y. Doctoral Faculty Award 1574, sound source. Other aspects of these various theoretical mechanisms have been discussed in detail elsewhere (Evans, 1973) and will not, therefore, be reviewed in this paper. Evans and Prescott (1962) postulated a dual sound source involving the laryngeal mechanism (arytenoepiglottic tube) for whistles, the nasal plugs with associated sacs for pulses. Norris (1964, 1969) seems to favor the nasal sac system for pulse pro- duction and, in general, a_ tissue-water transmission path in which the sound is projected through the “melon” into water. In addition he endorses the frequently sug- gested idea that the melon acts as an acoustic lens and functions in the forma- tion of the beam of sound. This theory has received additional support from the recent study by Norris and Harvey (1973) on sound transmission in the porpoise head and from the work of Vasanasi and Malius (1972). Recent measurements made using contact transducers on both the melon and the rostrum in two species in- dicate that echoranging pulses are pro- jected equally efficiently from both the rostrum and the melon. Analysis of data recorded with a multiple array of attached 130 1206 WILLIAM sensors places the source in the vicinity of the nasal plugs at a depth of 1.5-2.0 cm (Direcks et al., 1971). These data were used by Evans (1973) to propose a sound trans- mission path with both bone and adipose tissue components. A mechanical source without dependence on air flow, and thus independent of depth effects, could have definite advantages. Movements of the ex- ternal parts of the blowhole mechanism have been observed and discussed by several authors, e.g., Norris (1968) and Evans and Prescott (1962). Even though the paired muscular nasal plugs fit tightly into the external bony nares, they are capable of considerable movement. It is suggested that as these plugs are moved mechanically or pneumatically against the hard edge of the external bony nares, “relaxation oscil- lations,” with resultant acoustic puises, are generated by alternate resistance and re- lease of the plugs’ movements. The sound produced would thus follow the paths de- scribed by Norris and Harvey (1973); first, from the muscular plug through the melon and into the water; or second, from the plug through the melon, along the pre- maxillary bones, and radiate into the water from the tip of the rostrum. This is in con- irast to Purves’ (1967) contention that all the sound is radiated from the rostrum. The “relaxation-oscillation’”” mechanisms are appealing because of their efficient energy conversion capabilities, especially when one considers the sound levels mea- sured. However, such mechanisms would place certain demands on the tissues of the nasal region, notably with respect to toler- ance of shearing forces produced by high velocity air currents and the possible need for lubrication. We will now present new anatomical and histological data concern- ing the nasal pasages and diverticula of Turstops truncatus, which we believe rein- force the theory of sound production de- rived from acoustic studies. THE ANATOMY AND FUNCTION OF THE NASAL SAC SYSTEM The various theories previously discussed E. Evans AND PAUL F, A. MADERSON cast the nasal sac system in two possible extreme roles: that of the only active sound-producing system, or that of a reser- voir for storing “recycled” air during the underwater vocalizations produced by an- other structure, e.g., the larynx. In fact, all theories imply a partial “storage role” for some or all of the nasal system components. Consideration of the two extreme roles per- mits certain predictions to be made re- garding aspects of sac anatomy which can be investigated directly. If the sounds were produced solely in the larynx, with the sac system serving only as a reservoir for recycling, one would pre- dict a relatively simple system, of homo- geneous gross and microscopic structure lacking noteworthy localized specializa- tions. ‘This prediction is not borne out by such studies as those of Lawrence and Schevill (1956) or Mead (1972). If, on the other hand, the nasal sac system were assumed to be the source of the sounds, one would predict anatomical and histological diversity, with specializations appropriate to the various roles of the component elements. The odontocete nasal system is one which defies satisfactory verbal description and certainly reduction to two-dimensional graphic representation, although several excellent attempts to overcome the inherent complexities are available (Lawrence and Schevill, 1956; Evans and Prescott, 1962; Schenkkan, 1971; Mead, 1972). The hori- zontal section through the system of an adult T. truncatus shown in Figure 1 gives some indication of the problem. Fundamentally, the system consists of a single nasal passage, formed by the fusion of paired passages exiting the bony skull, running toward the dorsally situated “blow- hole,” with several pairs (the actual num- ber varying according to the species and the criteria of the investigator) of laterally arising diverticula. The entire system is bounded anteriorly by the nasal plug, a massive muscular organ which effects closure of the nasal passages (Lawrence and Schevill, 1956; Mead, 1972) and posteriorly by the assymetrical, concave, anterior sur- 131 DELPHINID SOUND PRODUCTION FIG. 1. A horizontal section across the nasal re- gion of Tursiops truncatus approximately 1.5 cm below the blowhole, viewed from the dorsal sur- face. Note that the section reveals the full length of the right posterior nasofrontal (tubular) sac (RPNF) and its junction with the right inferior vestibule (RIV), while the homologous left ele- ments lie approximately 1.0 cm ventral to this face of the cranium. The simplest possible representation of this system is shown in Figure 2, which also attempts to indicate the approximate inclinations of the various diverticula after their origin from the single nasal passage. ‘The “distortion” of this fundamental plan can be seen if Figure 2 is compared with Figures 1 and 3, which indicate that all the sacs and tubes are flattened to a greater or lesser degree, so that: (i) the epithelial surface area is greatly increased, and (ii) there is a high probability of actual temporary physical juxtapositioning of opposing epithelial sur- faces. If we add to these data the fact that fresh dissection material suggests a flex- ibility and mobility of the entire system comparable to that of the lips of a small boy making obnoxious noises, we can begin to appreciate how the sac system might produce sounds. Either theory of nasal sac function sug- gests that a column of air passes through the system at high speed. Since air pass- ing over an epithelial surface will exert a section. The grid lines are 3.8 cm apart. Other abbreviations: BL—blowhole ligament; LANF— left anterior nasofrontal sac; LVS—left vestibular sac; LPNF-—left posterior nasofrontal sac; RANF— right anterior nasofrontal sac; RVS—right ves- tibular sac; x—location of glandular tissue (Figs. 7, 8). The anterior nasofrontal sacs have flags in- serted in their lumina. lateral shearing force on the tissue, a priort one would predict that an anatom- ical arrangement minimizing epithelial sur- face area would be present. Furthermore, if the functions of the sac system were simply that of a reservoir for the recycling of a given volume of air, not only would simple gross anatomy be predictable, but one would expect epithelial homogeneity throughout the system. Neither of these predictions is fulfilled. In all genera, although variable from species to species, there is a pair of dorsal- most “‘vestibular sacs,” ventralmost “pre- maxillary sacs” (lying beneath the postero- ventral margin of the nasal plug), and be- tween them the “tubular sacs” (nasofrontal sacs) with anterior and posterior extensions (Fig. 2). The presence of distinct “accessory sacs’ (Schenkkan, 1971; Mead, 1972), “con- necting sacs” (Lawrence and_ Schevill, 1956), and paired “inferior vestibules”’ (Mead, 1972) seems to be somewhat variable and/or dependent on the interpretation of a particular investigator, but both are 132 1208 WILLIAM E. Evans AND PAUL F. A. MADERSON BLOWHOLE RIGHT VESTIBULAR SAC ANTERIOR =XTENSION Eee pe tee ee ee NASOFRONTAL / wen? Ok Slr: ia _ TUBULAR SAC “POSTERIOR EXTENSION INFEPIOR VESTIBULE LEFT PREMAXILLARY SAC RIGHT ACC ESSORY/ CONNECTING SAC 2 BONY NARES LEFT MARGIN OF BLOWHOLE LEFT VESTIBULAR SAC OPENING INTO NASA PASSAGE LEFT NASOFRONTAL SAC ANT. EXT. POST. EXT: INFERIOR VESTIBULE BLOWHOLE LIGAMENT po ae PREMAXILLARY SAC GLANDULAR REGION DIAGONAL MEMBRANE 133 DELPHINID SOUND PRODUCTION sufficiently distinct to be identified in T. truncatus. It is important to emphasize that not only is there variation in form and/or presence of all of the above- mention elements between genera and species, but that within at least one species—Delphinus delphis L.—there may be noticeable quantitative variation in size between individuals (Evans, unpublished). In all animals thus far studied, the right and left components not only show a rela- tive asymmetry of quantitative develop- ment which is characteristic of many aspects of odontocete head anatomy, but also show a spatial asymmetry with respect to the head axes in a manner which is not predicated by the bony elements. The entire nasal region is lined through- out by a stratified squamous parakeratotic epithelium which basically resembles that of the cetacean body epidermis (Spearman, 1972), although in the nasal region, the “corneous” layer is somewhat thinner. There are no indications of mucus-secret- ing or specialized sensory regions of any description. Lack of mucus-producing cells presumably reflects the fact that in an aquatic environment, the relative humidity of the air within the nasal system is always sufficiently high so that dessication is never a serious problem (Coulombe et al., 1965). The lack of sensory elements confirms the long-assumed anosmatic nature of the odontocete nose. The epithelia throughout have a general similarity to those of the human lips and buccal regions and _ this serves to reinforce the analogy of the potential for noise production by those parts of the human body. The histological structure of the epithelia throughout the nasal region can be divided into three broad categories. In _ those FIG. 2. A highly schematic representation of the nasal sac system of Tursiops truncatus viewed as a transparent object from the posterior aspect. Note that all axes are greatly distorted, and no attempt has been made to indicate the right/left asymmetry in terms of either size of homologous units, or with respect to spatial orientation. The position XX XXX indicates the location of the 1209 regions where the gross appearance is relatively smooth and unwrinkled and where the relationships of the epithelium to the underlying tissues suggest relative immobility, i.e., the ventralmost nasal pas- sages and the ventral aspects of the nasal plug leading into the premaxillary sacs, the epithelium is smooth, the cells are aligned parallel to the surface, and the dermal papillae are not very well developed (Fig. 4). In the vestibular sacs, which are conspicuously wrinkled, and which have been demonstrated to be capable of in- flation (Evans and Prescott, 1962), the epithelial histology is quite different (Fig. 5). The dermal papillae are well developed and are oriented perpendicular to the epithelial surface. The surface of the epithelium is crenate, and above each papillar apex, the corneal cells are arranged in regularly wavy rows. All features of the epithelium in the vestibular sacs suggest a functional adaptation directed primarily towards stretching, rather than to resist- ance to surface shearing forces seen in the first category (Fig. 4). The epithelial structure throughout the accessory sacs, inferior vestibules, and nasofrontal sacs varies between these two extremes (Fig. 6). The farther away from the actual nasal passage, the less determinate is the epithelial structure. This is particularly true as one approaches the blind ends of the anterior and posterior extensions of the nasofrontal sacs. Around the inferior vestibular surfaces, just extending into the posterior nasofron- tal sacs (Fig. 2), there are distinct modifi- cations of the epithelial structure (Mader- son, 1968). On the right side there are about 20, and on the left perhaps only half as many, crescentic pores approximate- blowhole ligament. Nomenclature after Lawrence and Scheville (1956) and Mead (1972). FIG. 3. A diagrammatic drawing of a sagittal sec- tion through the nasal region of Tursiops trun- catus taken at the axis Z-Z in Figure 2. An at- tempt has been made to show the general rela- tionships of the clements further to the left of the head. 134 A. MADERSON = 4 WILLIAM E. EVANS AND PAUL F., 1210 135 DELPHINID SOUND PRODUCTION ly 1.0 mm long (Fig. 7). These lead into compound acinar, exocrine glands, run- ning into the sub-epithelial tissues, which are larger on the right than on the left. Material in the acinar lumina probably derives by apocrine secretion from the sim- ple cuboidal epithelium. ‘The secreted material does not have mucinous proper- ties and may contain some lipid (Fig. 8). Similar structures have also been seen in Kogia, and Mead (1972) refers to “glandu- lar epithelia or tissues” in Inia geoffren- sis, Phocoena phocoena, and Phocoenoides dalli, but offers no histological descrip- tions. In all cases the location includes the inferior vestibular, nasofrontal sac tissues. DISCUSSION The acoustic data currently available suggest most forcibly that delphinid phona- tions are produced in the nasal region. ‘The figure of 1.5-2.0 cm beneath the blowhole margin provided by Diercks et al. (1971) as the site of origin would seem to corre- spond to the region where the lip of the nasal plug abuts the blowhole ligament (Fig. 8). While this location is only one of many which anatomical study shows close abutment of opposing epithelia, it is im- mediately adjacent to the glandular struc- tures, so that it is appropriate to consider the possible function of the latter. Their small total bulk suggests that they could not be salt glands, and their anatomy is so different from such organs (Waterman, 1971, p. 587) that they cannot be inter- preted as vestigial structures. They are similar in some ways to Steno’s glands found in other mammals (Moe and Boj- sen-Moller, 1971), but it is unlikely that they serve the humidifying function pro- posed by these authors. If we assume that 1211 sound production is effected by a relax- ation-oscillation mechanism involving rap- id intermittent juxtapositioning of the op- posing epithelia of the posterior nasal plug, and those of the ventral blowhole lga- ment, and circumnarial region in a rapid- ly moving airstream, then the glandular secretions could lubricate the tissues in- volved. and thus minimize mechanical damage. Other available anatomical data seem to strengthen this postulate. Gross and mi- croscopic analysis suggest that only the vestibular sacs regularly expand and de- flate, and Norris (1964) has indicated that not only could they serve as reservoirs for recycled air, but that this activity would also permit them to act as sound reflectors. Mead (1972) suggests, therefore, that the different sizes and shapes of the vestibular sacs in different species might permit dif- ferences in the shape of sound fields. Mead (1972) states that the premaxillary sacs “are probably the best situated for storage and recycling of air for sound production.” We suggest that their gross and microscop- ic structure does not reflect a distensible unit comparable to that of the vestibular sacs, but rather a mechanism permitting antero-postero movement of the nasal plug, ensuring a tight fit of the ventral aspect of the latter against the floor of the “sac” dur- ing intermittent contact of the posterior face with the blowhole ligament and the circumnarial tissues. Lawrence and Sche- vill (1956) suggested that the nasofrontal sacs (their “tubular sacs’) functioned as pneumatic seals around the nasal passage. We agree with Mead’s (1972) contention that this function could be better served by large muscle masses in the same area, and note his comment that in Grampus the left anterior nasofrontal sac is entirely FIG. 4. Photomicrograph of the epithelial struc- ture at the base of external nares in Tursiops truncatus. FIG. 5. Photomicrograph of the epithelial struc- ture of the left vestibular sac of Tursiops trun- catus. FIG. 6. Photomicrograph of the epithelial struc- ture of the posterior nasofrontal sac of Twrsiops truncatus. FIG. 7. Photomicrograph of the opening of a glan- dular duct in the right inferior vestibule of Tur- siops truncatus. FIG. 8. Photomicrograph of the distal acini of the gland shown in Figure 7. 136 1212 WILLIAM E. EvANs AND absent. While the intra-specific variation which we have commented upon has not yet been quantified, it seems most unlikely that any significant variation would be “permitted” by natural selection if the nasofrontal sacs played any active major role in such a sophisticated function as delphinid phonation. Schenkkan (1971) and Mead (1972) both draw attention to the considerable diversity in structure and degree of development of the accessory sacs and vestibular regions between gene- ra. Mead (1972) makes frequent reference to the possibility that any and all diver- ticula could function as storage areas for recycled air. However, in the light of Nor- ris’ (1964) suggestion that an inflated ves- tibular sac could act as a sound reflector, it is important to note that if the naso- frontal-vestibular accessory region did_ be- come wholly or partially filled with air, then we would assume that they would play a similar reflecting role. According to this premise there should be a relationship between the details of the presence and de- gree of development of these various com- ponents and the shape of the sound field produced by particular genera. Since there are insufficient data available to establish such a relationship, it is simpler to assume that air storage is not the primary func- tion of these diverticula. Our histological data, derived from stud- ies on Tursiops and Kogia, and comments by Mead (1972) on the other genera, sug- gest that glandular secretion is an impor- tant function of the vestibular-nasofrontal regions. We have suggested that lubrica- tion of the posterior nasal plug tissues might be the function of these secretions. We have also indicated that it may be the vestibular sacs alone which serve as re- cycling storage areas. Therefore, the high- speed current of air which passes up the paired narial openings towards the ves- tibular sacs might tend to blow the glan- dular secretions back up the nasofrontal system, thus deflecting them away from the surfaces which should be lubricated. How- ever, Mead (1972) suggests that the intrin- sic musculature of the nasofrontal sacs Paut F. A. MAnpERSON would permit their emptying and filling. Therefore, if we assume that the functions of the nasofrontal-vestibular accessory re- gions are secretory, and also storage of the secreted materials, we can propose the fol- lowing answers to some of the problems which have been raised. During periods of non-sound production, the opening of the vestibular-nasofrontal accessory system into the nasal passage could be occluded by the nasal plug being drawn back tightly against the blowhole ligament (Fig. 2). During this time, glandular secretions could accu- mulate within the lumina, especially of the nasofrontal sacs due to relaxation of the intrinsic musculature. During sound _pro- duction, anterior movement of the nasal plug would permit expression of the glan- dular secretion which, aided by active ex- pulsion by contraction of the intrinsic mus- culature, would not only lubricate the op- posing epithelial surfaces, but possibly also prevent the entry of air into this system of diverticula. This explanation satisfies the problem of the possibility of air-filling creating an acoustic reflector, but, should it be proven that there is indeed a correla- tion between vestibular-nasofrontal acces- sory anatomy and the shape of the sound fields in different genera, the model can be modified without altering the funda- mental functions proposed here. CONCLUSIONS Following an extensive review of the nasal anatomy of a variety of odontocete genera, Mead (1972) states: “In summary, it appears that the structures most likely to be involved in sound production are those in the vicinity of the nasal plugs.” We have found that this premise is sup- ported by recent acoustic studies (Diercks et al., 1971; Evans, 1973) and by certain anatomical specializations adjacent to these tissues described in the present paper. Fur- ther substantiation of the model presented here must await demonstration of specia- lized glandular structures in similar regions in all other sound-producing genera, his- tochemical identification of the secretions 137 DELPHINID SOUND PRODUCTION produced by analysis of fresh material, and finally, correlations between the anatomi- cal diversity now known to exist between genera and species and the acoustic prop- erties of the sounds produced by them. REFERENCES Coulombe, H. N., S. H. Ridgway, and W. E. Evans. 1965. Respiratory water exchange in two species of porpoise. Science 149:86-88. Diercks, J. J.. R. T. Trochta, R. L. Greenlaw, and W. E. Evans. 1971. Recording and analysis of dolphin echolocation signals. J. Acoust. Soc. Amer. 49:1729-1732. Evans, W. E. 1973. A discussion of echolocation ‘by cetaceans based on experiments with marine delphinids and one species of freshwater dolphin. J. Acoust. Soc. Amer. 54:191-199. Evans, W. E., and J. H. Prescott. 1962. Observa- tions of the sound production capabilities of the bottlenose porpoise: a study of whistles and clicks. Zoologica 47:121-128. Lawrence, B., and W. E. Schevill. 1956. The func- tional anatomy of the delphinid nose. Bull. Mus. Comp. Zool. (Harvard) 114:103-151. Maderson, P. F. A. 1968. The histology of the nasal epithelia of Tursiops truncatus (Cetacea) with preliminary observations on a series of glandular structures. Amer. Zool. 8:810. (Abstr.) Mead, J. G. 1972. On the anatomy of the external nasal passages and facial complex in the family Delphinidae of the order Cetacea. Doctoral Thesis, Univ. of Chicago. Moe, H., and F. Bojsen-Moller. 1971. The fine structure of the lateral nasal gland (Steno’s 1213 gland) of the rat. J. Ultrastruct. Res. 36:127- 148. Norris, K. S. 1964. Some problems of echolocation in cetaceans, p. 317-336. In W. N. Tavolga [ed.], Marine bioacoustics. Pergamon Press, New York. Norris, K. S. 1968. The evolution of acoustic mech- anisms in odontocete cetaceans, p. 297-324. In E. T. Drake [ed.], Evolution and environment. Yale Univ. Press, New Haven. Norris, K. S. 1969. The echolocation of marine mammals, p. 391-423. In H. T. Anderson [ed.], The biology of marine mammals, Academic Press, New York. Norris, K. S., and G. W. Harvey. 1972. A theory for the function of the spermaceti organ of the sperm whale (Physeter catodon, L.), p. 397-417. In Animal orientation and navigation, NASA SP-262, Sci. and Tech. Office NASA, Washington, D.C. Norris, K. S., and G. W. Harvey. 1973. Sound trans- mission in the porpoise head. Science (In press) Purves, P. E. 1967. Anatomical and experimental observations on the cetacean sonar system, p. 197-270. In R. G. Busnel [ed.], Animal sonar sys- tems, biology and bionics. Imprimerie Louis- Jean, GAP, Haute-Alpes. Schenkkan, E. J. 1971. The occurrence and posi- tion of the “connecting sac’ in the nasal tract complex of small odontocetes (Mammalia, Cetacea). Beaufortia 19:37-43. Spearman, R. I. C. 1972. The epidermal stratum corneum of the whale. J. Anat. 113:373-381. Vasanasi, V., and D. C. Malius. 1972. Triacylglycer- ols characteristic of porpoise acoustic tissues: molecular structures of dilsovaleroylglycerides. Science 176:4037, p. 926-928. Waterman, A. J. 1971. Chordate structure and function. Macmillan, New York. 138 MORPHOLOGY AND PHYLOGENY OF HAIR By Charles R. Noback* Department of Anatomy, College of Physicians and Surgeons, Columbia University, New York Hair is a structure found exclusively in mammals. With this in mind, Oken named the Mammalia, Trichozoa (hair animals), and Bonnet (1892) named them Pilifera (hair bearers). Of the many aspects of morphology and phylogeny of hair, only four will be discussed. These include (1) the principle of the arrangement of hairs in group patterns, (2) the types of hair and their relation to the principle of the group pattern, (3) a brief analysis of the structural elements of hair and their relation to the types of hair, and (4) the phylogeny of hair, with some remarks on (a) the relation of hair to the epidermal derivatives of other vertebrate classes and (0) aspects of the phylogeny of the hair and wool of sheep to illustrate that marked differences in hair coats exist between closely related animals. Hair is the subject of a voluminous literature. Toldt (1910, 1912, 1914, and 1935), Danforth (1925a), Pinkus (1927), Pax and Arndt (1929-1938), Trotter (1932), Lochte (1938), Smith and Glaister (1939), and Stoves (1943a) discuss the problem of mammalian hair in general. Wildman (1940), von Bergen and Krause (1942), and the American Society for Testing Materials (1948) discuss the problem of fiber identification as applied to textiles. Principle of the Group Pattern of Hairs In the only extensive survey of the grouping of hair in mammals, DeMei- jere (1894) documented the concept of the group pattern of hair (FIGURES 1-6). Unfortunately, the few studies on this phase of the problem since that time have not fully exploited the implications of this concept. DeMei- jere concluded that hairs are mainly arranged in groups with the pattern of 3 hairs—with the largest hair in the middle—as the basic pattern. The concept of the basic trio as the primitive condition is accepted as an ade- quate working hypothesis by Wildman (1932), Galpin (1935), Héfer (1914), Gibbs (1938), Hardy (1946), and others. DeMeijere described 8 patterns: (1) 3 or less hairs behind each scale of the tail (as in the opossum, Didelphis marsupialis), (2) more than 3 hairs behind each scale of the tail (as in the rodent, Loncheres [Echimys] cristata), (3) 3 hairs (as in the back of the marmoset, Midas rosalia), (4) more than 3 hairs arranged in a regular pattern with some of greater diameter than others (as in the back hairs of Loncheres |Echimys] cristata in FIGURE 3), (5) several hairs composed of a number of fine hairs and one coarse hair (as in the back of the dog, Canis familiaris, in FIGURE 5D), (6) several hairs composed of a number of fine hairs and one isolated coarse hair (as in the back hairs of the mouse, Mus decumanus, in FIGURE 6D), (7) scatterings of fine hairs with no apparent * The author wishes to thank Dr. Margaret Hardy, Division of Animal Health and Production, Sydney, Australia, for her valuable suggestions. 476 139 Noback: Morphology and Phylogeny 477 arrangement and a few intermingled coarse hairs (as in the back hairs of the cat, Felis domesticus in FIGURE 4D), and (8) hairs in irregularly scattered groups (as in the back hair of the raccoon, Procyon cancrivorus). Dawson (1930) does not completely agree with DeMeijere’s pattern in the guinea pig. She found variations in the pattern and no correlation be- tween the size of hair and the arrangement of the hairs in each group. Histological study frequently shows follicle grouping which was not appar- ent to DeMeijere when he was examining only the skin surface, e.g., in Felis domesticus (see Hofer, 1914). This indicates that analyses of the group pattern of hairs are needed in both common laboratory mammals and mammals in general. In addition, DeMeijere analyzed the formation of the patterns by ex- amining the skins of animals during their development (FIGURES 4-6). This phase of the problem has been extended to include a study of the ontog- eny of the arrangement of hair follicles in sheep (Wildman, 1932, Galpin, 1935, and Duerden, 1939), in the cat (Hofer, 1914), in marsupials (Gibbs, 1938, Stoves, 1944b, and Hardy, 1946), in the mouse (Calef, 1900, Dry, 1926, and Gibbs, 1941) in the rat (Frazer, 1928), and in a number of mam- mals (Duerden, 1939). The terminology used by these authors in this problem is summarized in TABLE 1 (adapted from Wildman and Carter, 1939 and Carter, 1943). Utilizing the terminology of Wildman and Carter, 1939, the following is a brief statement of the relation of the fiber generations. The first follicles to differentiate are the central trio follicles (FIGURE 7). If these follicles appear at two different times as in the opossum (Gibbs, 1938), then the follicles are called ‘primary X”’ and “primary Y.”” The essential point is that each of these primary follicles will be the central follicle of different hair groups. Later in development, other follicles of the hair group differentiate in relation to these central trio follicles. The trio is formed when two follicles are differentiated lateral to the primary follicles (FIGURE 8). The lateral follicles associated with primary X and primary Y are called re- spectively “primary x” and “primary y.’”’ If only one lateral follicle is formed adjacent to a primary follicle (X or Y), then a couplet follicle is formed. If no lateral follicles differentiate, a primary follicle (X or Y) is called a “‘solitary follicle.” Later, another generation of follicles is differ- entiated—the secondary follicles. In the opossum (FIGURE 9), these secondary follicles are located between the central trio follicle and the lateral trio follicles. The ontogenetic studies of follicle arrangement have added confirmatory evidence to DeMeijere’s basic concept that in mammals there is a universal and regular grouping of hair follicles (Hardy, 1946). In general, the early differentiating follicles (central trio follicles) form the coarse overhair, while the late differentiating follicles (lateral trio follicles and secondary follicles) form the fine underhair. Lateral trio follicles sometimes at least produce overhair like that of the central fol- licles (e.g. in sheep) or intermediate types such as awns, which are classified by Danforth (1925a) as overhair. In Ornithorhynchus anatinus (Spencer and Sweet, 1899) and many marsupials (Gibbs, 1938, Bolliger and Hardy, 140 478 Annals New York Academy of Sciences 1945, Hardy, 1946), however, the lateral trio fibers are indistinguishable from those of secondary follicles, so it is difficult to place them in either the “overhair” or the ‘‘underhair” category. FIGURES 1-9 (see facing page). Spencer and Sweet (1899) claimed that, in monotremes, each group of follicles was differentiated by budding from the central follicle. This has not been described in marsupials or in eutherians, in which the follicles arise independently as epidermal downgrowths. Monotremes and mar- 141 Noback: Morphology and Phylogeny 479 suplals have in common the fact that a follicle group typically contains a large central follicle with a sudoriferous gland, and two or more clusters of smaller lateral follicles (Spencer and Sweet, 1899, Gibbs, 1938, Hardy, 1946). This arrangement is also found in some eutherians, such as the cat (H6fer, 1914) and dog (Claushen, 1933). Inthe cat and a few other eutherians, the first-formed lateral follicles (primary x and y of the classification of Wild- man and Carter, 1939) produce hairs intermediate in type between those of the central and the other lateral follicles. There are other eutherians in which the lateral primary x and y fibers are still more like the central pri- mary X and Y fibers, asin the pig (Héfliger, 1931) and the sheep (Carter, 1943). Except in the rodents, there is always a sudoriferous gland opening into the central primary X or Y follicle (Hardy, unpublished data). Many animals, such as the pig and sheep, also have a sudoriferous gland opening into each primary x and y follicle, but others do not (Duerden, 1939). Some of the eutherians have only primary follicles in their skin, each with a sudoriferous gland. Findlay and Yang (1948) showed that this is the arrangement in cattle, and the same is probably true in horses and in human head hair (Hardy, unpublished observations). Types of Hair DeMeijere’s analysis leads to the classification of hair types by Toldt (1910 and 1935) and by Danforth (1925a). Many details of the hair types in many species of animals and the variations of the structure of these types are described, illustrated, and bibliographically annotated by Toldt (1935) and Lochte (1938). Types OF MAMMALIAN HAIR (after Danforth, 1925a) 1. Hairs with specialized follicles containing erectile tissue. Large, stiff hairs that are preeminently sensory. They have been variously designated as feelers, whiskers, FIGuRES 1-9 (see opposite page). FicurE 1. The trio hair group pattern on the back and tail of the marmoset, Midas rosalia (after DeMei- jere, 1896). All hairs have similar diameters. Ficure 2. The hair group pattern of more than 3 hairs with some fibers of greater diameter than other fibers on the back of the paca, Coelogenys paca (after DeMeijere, 1896). Ficure 3. The hair group pattern of more than 3 hairs with some fibers of greater diameter than other fibers on the back of the rodent, Loncheres (Echimys) cristata (after DeMeijere, 1896). Ficure 4. Ontogeny of a hair group on the back of the cat, Felis domesticus. A, froma newborn animal; B and C, from an older animal; and D, from an adult animal (after DeMeijere, 1896). FicurE 5. Ontogeny of a hair group on the back of the dog, Canis familiaris. A, from an embryo dog; B, from a newborn animal; C, froma young dog; and D, from an adult animal (after DeMeijere, 1896). Ficure 6. Ontogeny of a hair group on the back of the mouse, Mus decumanus. A, froma7 cm. long ani- mal; B, from a 9 cm. long animal; C, from a 12.5 cm. long animal; and D, from an adult animal. (Ficures 4, 5, and 6 illustrate that the follicle of the first hair to erupt (A) will be the follicle of the coars- est hair of the hair group in the adult. The type of hair group pattern in the adult (D) in each figure is noted in the text. The X in the diagrams marks the location of pubis follicles.) FicureE 7. The primary follicles X (the more differentiated follicles) and the primary follicles Y (the less differentiated follicles) in the transverse section of skin of a 12.5 cm. Australian opossum embryo (Trichosurus vulpecula). Follicles are scattered irregularly. (After Gibbs, 1938.) . FiGurRE 8. Two new follicles (primary x or primary y) have become grouped with each previously differen- tiated follicle (primary X or primary Y) to form the typical trio arrangement. The trio would be either primary x, primary X, primary x or primary y, primary Y, primary y. Transverse section of skin of a 15.0 cm. Australian opossum embryo (Trichosurus vulpecula). (After Gibbs, 1938.) FicurE 9. Two secondary follicles have added to each frio group to forma 5 follicle group. The secondary follicles differentiate between the primary X (or Y) follicle and the primary x (or y) follicles. The five group would be either primary x, secondary follicle, primary X, secondary follicle, primary x or primary y, second- ary follicle, primary Y, secondary follicle, primary y. Transverse section of skin from 20.0 cm. Australian opossum embryo (Trichosurus vulpecula). Note presence of a dermal capsule surrounding each 5 follicle group. (After Gibbs, 1938.) . (In FIGURES 7, 8, and 9, the terminology of Wildman and Carter (1939), noted in the text, is used.) 142 Annals New York Academy of Sciences 480 "(6£61) JaJ1eD pue ueWIP]IAA WoOly paidopy * Sapo} IeeYLog Sap [O} Avutoyenb SO[IJOF [VIII] Sa[IT[JO} O11}-}sod AIOF | Buoy A SefNley PHOS SEPM SO[ITJOJ TVVYWUWL}S | O11] [esaIVT | IjIT]JOF xX AVI} [U419} RB] 9BIP] OI} [R1I} RY] JEM a es Aldepuosas AIVPUOIIS le (AR Iain ee Sd ed oat IP YfOF ABBYPONYY Arewiid fapyfoy Xx Areutid 9] JOJ [VsyUad Old} [B}Uad Gd ped bed ed (109) (FI61) 49f9H (aay) (qaays) é balan a (sjo1dnsaput) (aus) UD (SIDUMIUD sso S i 761 Heep ne ee a (Otol) “pany (6£61) uapaang snolapa) (F161) 1PJ0] XA Areuud Jo ¥ Aivunid A+ x Arewtid x + y Areuud A Arewiud x Arewid A Azewud Sapo [O} ATBpuodag SI}! [0] Are] (P) rad boas USE) yojdno,) (9) SOIT [OJ Ol} [eae] (4) SEE MMLes XY Aqwuind oy pesjuady (ke) sopdffo} AIvUTI (6£61) 42140.) pun upwpyt 4 ,VIIVNNVIJY AHL NI AOOTONINAAL AIOITIOJ-AAGI A ] alav 143 Noback: Morphology and Phylogeny 481 sensory hairs, sinus hairs, tactile hairs, vibrissae, etc. They occur in all mammals except man, and are grouped by Botezat (1914) (Pocock, 1914) essentially as follows: (1). Active tactile hairs—under voluntary control. (2) Passive tactile hairs—not under voluntary control. (a) Follicles characterized by a circular sinus. (6) Follicles without a circular sinus. 2. Hairs with follicles not containing erectile tissue. The remaining types of hair, most of which are more or less defensive or protective in function. In many cases, the follicles have a good nerve supply, endowing the hair with a passive sensory function as well. These hairs are grouped here according to their size and rigidity. (1). Coarser, more or less stiffened ‘‘overhair,” guard hair, top hair. (a) Spines. Greatly enlarged and often modified defensive hairs, quills. (b) Bristles. Firm, usually subulate, deeply pigmented, and generally scattered hairs. ‘Transitional hairs’? (Botezat, 1914), ‘‘Leithaare’”’ (Toldt, 1910), “protective hair,” “primary hair,” ‘‘overhair.’’ This group also includes mane hairs. (c) Awns. Hairs with a firm, generally mucronate tip but weaker and softer near the base. ‘‘Grannenhaare”’ (Toldt, 1910), “‘overhair,”’ ‘“pro- tective hair.” (2). Fine, uniformly soft “underhair,” ‘‘ground hair,” ‘“‘underwool.” (a) Wool. Long, soft, usually curly hair. (6) Fur. Thick, fine, relatively short hair—‘‘underhair,” ‘‘wool hair.” (c) Vellus. Finest and shortest hair—‘‘down,” ‘‘wool,”’ ‘‘fuzz,” “lanugo.’ (Danforth, 1939). 23) 166 66 7 The following comments supplement the above classification. The guard hairs are listed in a series from greater to lesser rigidity (in order: spines, bristles, and awns). There are many intergrade hairs between the typical bristle and the typical awn and between the typical awn and the typical fur hair (FIGURES 10, 11, and 12). The tactile hairs have a rich nerve supply, while the roots of some are encircled by large circular sinuses containing erectile tissue. When the pressure in the circular sinus is increased the hair becomes a more efficient pressure receptor. The overhairs have a definite nerve supply, while the underhairs have no direct nerve supply. As a general but not absolute rule, the coarser hairs appear ontogenetically earlier than the finer hairs (Gibbs, 1938, Danforth, 1925a, Duerden, 1937 (reported by Wildman, 1937), Hofer, 1914, and Spencer and Sweet, 1899). The contour, diameter, and shape of a hair fiber changes from its root to its tip (Note awns, FIGURES 16-18). The cross-sectional outline of hairs may vary from the thick rounded porcupine quill to the eccentric flattened hairs of seals. The former serves a protective function, while the latter is adapted to hug to the skin so as not to hinder aquatic locomotion. Many details of the anatomy of hair form are noted by Stoves (1942 and 1944a), Toldt (1935), and Lochte (1938). It is possible for a hair follicle to differentiate one type of hair at one stage and another type at another stage. The follicle of a bristle (kemp) of the Merino lamb may become the follicle of wool in the adult sheep (Duerden, 1937, reported by Wildman, 1937). A fine lanugo hair of the human fetus is associated with a follicle which will later be the follicle of a coarser hair. The theories of hair curling are reviewed by Herre and Wigger (1939). The curling of hair in primitive sheep is independent of the arrangement of hair, existence of hair whorls, or the cross section of the hair (Pfeifer, 1929). 144 482 Annals New York Academy of Sciences Wildman (1932) suggests that the shape of the follicle, especially the curve in its basal portion, is a possible factor in hair curling. Reversal of the spiral in some wool fibers may be explained according to Wildman as due to a shift in the growing point of the follicle and inner root sheath. Spiral reversal occurs in human hair (Danforth, 1926). Pfeifer (1929) doubts that curling is determined by a curve of the follicle alone and suggests that Tiinzer’s (1926) contention that the follicle must be saber-shaped is im- lO ll \ \D ce GA ooo oo (FP E72208 9 s 3 - io) [ -D C l=) sin FicureEs 10-15. Ficure 10. The hair of the fox, Canis vulpes (after Toldt, 1935), illustrating intergrade hairs. From the left to the right, Toldt named the fibers Leithaar (bristles), Leit-Grannenhaar, thick Grannenhaar (awns), thin Grannenhaar, Grannen-Wollhaar, and Wollhaar (fur). Ficure 11. The hair of the chinchilla, Chinchilla laniger (after Toldt, 1935) illustrating an animal hair coat with hairs of approximately the same length. The 2 hairs on the left are awns, and the rest, either intergrade hairs or fur hairs. Ficure 12. The hair of the wild pig, Sus scrofa (after Toldt, 1935) illustrating bristles on the left and Hoda at on the right with some intergrade hairs between them. Note the brushlike distal ends of the ristles. FicurE 13. The scale index (S. I.), according to Hausman (1930), is equal to the ratio of the free proximo- distal length of a scale (F) to the diameter of the hair shaft (D). FicureE 14. The thickness of the cuticle (C. T.), according to Rudall (1941), is equal to the length of a cuticular scale (1) times the sine of angle (sin ©) the scale makes with the cortex (X). FicuRE 15. Cross sections of several regions of a fur hair (left) and an awn (right) of the rabbit (after Toldt, 1935). The sections, at the top of the figure, are from the base of the hair and, at the bottom of the figure, from the tip of the hair. Illustrates general uniformity of the diameters of the fur haii and differences in diameters and contour of awn hairs throughout their lengths. 14 I5 9 9a portant. Waving of all compact wools is due at least in part to the flat- tening of the primary spiral and to the unequal lateral growth of the fiber (Duerden, 1927). The curling of hair in karakul sheep fetuses may be associated with the differences in the rates of growth in the various skin layers (Herre and Wigger, 1939). The factors responsible for curling and crimping of hair are as yet not completely known. 145 Noback: Morphology and Phylogeny 483 Structural Components of Hair The cuticle, cortex, and medulla are the three structural components in hair. They will be discussed in order. Cuticle. The cuticle consists of thin, unpigmented, transparent over- lapping scales, whose free margins are oriented toward the tip of the hair I6 7 I8 | ! ni | | AAA OUT RR NAH DA WIAA her 20 al | ROR fs SAAN FIGURES 16-21. FicuRE 16. Diagram of the fiber components of coat of a generalized non-wooled animal (after Duerden, 1929). Note presence of bristles (coarse fibers), awns (fibers with fine basal segments and coarse distal segments) and fur fibers (fine fibers). Figure 17. Diagram of the fibers of the wild sheep (after Duerden, 1929). Note the presence of bristles (kemp), awns (heterotypes), and wool. FiGuRE 18. Diagram of the fibers of British mountain breeds (after Duerden, 1929). The fibers are mainly awns and wool. Few bristles are present. FicurE 19. Diagram of the fibers of the British luster breeds (after Duerden, 1929). Fibers on the left are wool fibers which are coarser than the wool fibers of wild sheep. The fibers on the right are modified awns with fine proximal segments and slightly coarse distal segments. All fibers are elongated and spiraled. Ficure 20. Diagram of fibers of adult Merino sheep (after Duerden, 1929). All fibers are wool. Note uniformity of all fibers as to size, length, and waviness. These wool fibers are coarser than wool fibers from wild sheep. Unlike the fibers of other breeds, the fibers of the adult Merino sheep grow from persistent germs and do not shed. FicureE 21. Diagram of the fibers of the Merinolamb. Note the presence of bristles (kemp), awns (hetero- types), and wool. During later development, the bristles are shed and the distal coarse segments of the awns are lost. The adult coat is formed by the persistent growth of the wool fibers of the lamb, by the re- placement of wool in the follicles of the shed kemp, and by the persistence of the growth of the proximal seg- ments of the awns. (FIGURE 22). Within the follicle, the free margins of the hair cuticular scales interlock with the inner root sheath cuticular scales, which are oriented in the opposite direction toward the papilla. This interlocking of scales helps to secure the hair in place (Danforth, 1925a). The cuticle functions as a capsule containing the longitudinally splitable cortex (Rudall, 1941). This explains why the cortex of a hair frays at its severed end. In addition, the cuticle, with its oily layer, prevents the transfer of water (Rudall, 1941). 146 484 Annals New York Academy of Sciences The cuticular scales vary in thickness from 0.5 to 3 micra (Frolich, Spétel, and Tanzer, 1929). Since the scales overlap, the number of overlapping scales at any point on the hair surface determines the thickness of the cuticle. The cuticular thickness may be expressed as being equal to the length of the scales times the sine of the angle the scale makes with the cortical surface (FIGURE 14, Rudall, 1941). The cuticular scales may be classified into two types: coronal scales and imbricate scales (Hausman, 1930). A coronal scale completely encircles the hair shaft. They are subdivided according to the contour of the free margins as: simple, serrate, or dentate (FIGURE 23). Miiller (1939) con- tends that a coronal scale is in reality several scales whose lateral edges are HAIR SHAFT IN MICRONS 200 ononar | ACUMINATE | entice | ELONGATE OVATE FLATTENED FicureE 22. Graph illustrating the relation of the diameter of the hair to the ore of cuticular scales. The finest hairs (with small diameters) have a high-scale index and coronal scales. he coarsest hairs (with large diameters) have a low-scale index and flattened scales. Diameters of hair shafts are plotted on the ordinate. General regions of the occurrence of scale forms are shown along the abscissa, the average scale indices along the curve. The figures of the scale types beneath the graph are not drawn to scale. (After Hausman, 1930.) fused. For example, a dentate coronal scale with 5 processes in its free border is the fused product of 5 elongated pointed scales. An imbricate scale does not completely surround the hair shaft. They are classified as ovate, acuminate, elongate, crenate, and flattened (FIGURE 22, Hausman, 1930). Hausman (1930) devised a scale index to express the relation between the diameter of the hair shaft and the free proximo-distal dimension of the scales (FIGURE 13). The free proximo-distal dimension is actually a means of expressing the type of scale. For example, coronal scales have a large proximo-distal dimension, while crenate scales have a small dimension (FIGURE 22). An analysis of the scale indices indicates that a relation exists between the types of scales and the shaft diameters. In general, the finest 147 Noback: Morphology and Phylogeny 485 hairs have large scale indices and coronal scales, while the coarsest hairs have small scale indices and crenate or flattened scales. On the basis of the above, it is concluded that the types of cuticular scales present on hair are related not to the taxonomic status of the animal possessing the hair but rather to the diameter of the hair shaft (Hausman, 1930). In hairs with both thick and thin segments, the thick segments have the scale types of large diameter hairs while the thin segments have the scale types of small diameter hairs. A coarse guard hair has scales with free lips that are closely applied to the cortex and are scarcely raised. As a result, these hairs have a high luster (due to unbroken reflection of light from the hair surface) and do not inter- lock with other hairs. A fine underhair has scales with lips that have raised margins. Asa result, these hairs are dull (due to broken reflection of light) and interlock with other fine hairs. Thus, mohair has a high luster but makes poor felt, while wool is dull but makes good textiles. A. B. C. Ficure 23. Figures illustrating the types of coronal cuticular scales. A. simple scales, B. serrate scales, C. dentate scales, (after Hausman, 1930). Note raised margins on the free lips of scales. Many details of the cuticle.in many species of animals are presented and illustrated by Lochte (1938). Cortex. The cortex usually forms the main bulk ofa hair. It isa column of fusiform keratinized cells which are coalesced into a rigid, almost homoge- neous, hyaline mass (Hausman, 1932). Damaged hairs tend to split length- wise because the elongated cortical cells are oriented longitudinally. The cortex has such a low refractive index—due to the degree of cornification— that, in the absence of pigment, it is translucent. Since cortical scales have not been analyzed in such detail as cuticular scales, no statement can be made of a relation between cortical scale morphology and hair size. The form and distribution of the pigment in the cortex and the medulla is noted by Lochte (1938), Toldt (1935), and Hausman (1930). Hausman (1932 and 1944) analyzed the cortical air spaces known as cortical fusi—cortical in location and fusiform in shape—air vacuoles, air chambers, air vesicles, or vacuoles. As the irregular-shaped cortical cells located in the bulb rise to the follicular mouth, they carry between them cavities filled with tissue fluid. As the hair shaft dries out, the cavities lose 148 486 Annals New York Academy of Sciences the fluid, and air may fill the resulting spaces—the fusi. The shape of the fusi vary. They are largest, most numerous, and most prominent near the base of the hair, and they are filiform and thin or lost in the distal seg- ments of the hair. Seldom do they persist to the tip of ahair. As a rule, they are visible only under a microscope. Hausman implies that there is a relation between fusi and hair size. Presumably, the coarser a hair seg- ment is, the more numerous the fusi. Ringed hair results when the fusi appear in masses at regular intervals in the shaft. Fractured fusi result when hairs are damaged sufficiently to separate the cortical cells enough to allow air to collect between them. Fusi can be distinguished from pigment granules, for they are fusiform, whereas pigment granules have blunt ends. The presence of a thin membrane located between the cuticle and the cortex has been assumed by Lehmann (1944). Observations of pigment granules, cell nuclei, and submicroscopic fibrils are presented by Mercer (1942), Hausman (1930), and others. Medulla. The medulla (pith), when present, is composed of shrunken and variably shaped cornified remnants of epithelial cells connected by a fila- mentous network. In contrast to the cortex, the medulla is less dense and has fewer and larger cells, which are more loosely held together. In the medulla are air cells or chambers, which are filled by a gas, probably air. These air cells may be intracellular (deer) or intercellular (dog, weasel, and rat) (Lochte, 1938). The intercellular air cells are classifiable accord- ing to their coarseness and arrangement (Lochte, 1934 and 1938). Medullas are classified by Hausman (1930) as follows: absence of medulla, discontinuous medulla (air cells separate), intermediate medulla (several separate air cells of the discontinuous type arranged into regular groups), continuous medulla (air cells arranged to form a column), and fragmental medulla (air cells arranged into irregular groups). These types are illus- trated in FIGURE 24 and are arranged in the order of the sizes of hairs in which they are located. In the finest hairs (underfur), the medulla is either absent or of the discontinuous type. In the coarsest hairs, the medulla is either of the continuous or the fragmental type (FIGURE 24). If a hair varies in thickness, its medulla will vary. For example, in the awns of sheep, the distal thickened segment has a medulla, while the fine proximal segment may have no medulla. The arrangement of the medullary air cells is related not to the taxonomic group of the animal possessing the hair nor the age of the hair, but rather to the diameter of the hair shaft (FIGURE 24) (Hausman, 1930; Wynkoop, 1929; and Smith, 1933). The sheens and colors of hairs are largely determined by the light reflected from the medulla (Hausman, 1944), Although the cortex forms the bulk of the shaft in most hairs, the medulla assumes large proportions in some hairs. In rabbit hair (FIGURE 15), the medulla is composed of large air cells separated by little more than a frame- work of cortex (Stoves, 1944a). The significance of the cuticle, cortex, and medulla in the commercial aspects of fur is presented by Bachrach (1946). Although many of the 149 Noback: Morphology and Phylogeny 487 details of the structural elements of hair cannot be definitely utilized to identify an animal species (Hausman, 1944), it is possible that some morpho- logical features of hair can be used (Williams, 1938). Some chemical and physical aspects of the morphological elements of hair have been analyzed. Not only do the cuticle, cortex, and medulla exhibit different chemical and physical properties, but various segments of these structural elements may have different chemical and physical proper- FRAGMENTAL FicurE 24. Graph illustrating the relation of the diameter of the hair to the types of medullas. The finest hairs have no medulla, and the coarsest hairs have a fragmental medulla. Diameters in micra of the hair shafts are plotted on the ordinate. The figures of the types of medullas beneath the graph are not drawn to scale. (After Hausman, 1930.) ties (Rudall, 1944; Stoves, 19434, 1945; Lustig, Kondritzer, and Moore, 1945; Leblond, 1951; and Giroud and Leblond, 1951). Some Phylogenetic Aspects of Hair The relation of hair to the epidermal structures in non-mammalian ani- mals has been discussed by many authors and has been summarized by 150 488 Annals New York Academy of Sciences Botezat (1913 and 1914), Danforth (1925b), and Matkeiev (1932). No direct relation between hair and non-mammalian epidermal elements has been established. Hair is most probably an analog to these structures. Danforth (1925b) and others conclude that hair is probably a de nove morpho- logical entity in mammals. Broili (1927) reports that he identified hair and hair follicles in a fossil aquatic reptile, Rhamphorynchus. This animal is a specialized reptile, removed from those reptiles in the evolutionary line to mammals. If established, this observation would alter the concept that only mammals produce hair. The phylogeny of hair in related groups of animals has not been analyzed extensively. Because of the economic importance of wool, several studies of the hair types in the coat of a number of breeds of sheep have been made. One significant aspect of these studies is that they illustrate how the hair coat may vary in closely related forms. This statement is adapted primarily from Duerden (1927 and 1929). The generalized wild animal hair coat consists of an overcoat of bristles and awns and an undercoat of fur (FIGURE 16). In the wild sheep and the black-headed Persian sheep, the hair coat is similar to that of the wild animal. These sheep have an overcoat of bristles (called kemp) and awns (called heterotypes) and an undercoat of wool (FIGURE 17). The British mountain breeds have a hair coat consisting of awns and wool (FIGURE 18). In these breeds, kemp formation is negligible. The coat of the British luster breeds have evolved in another direction. The awns retain their fine proximal segments. Their distal segments are still thicker than the proximal segments, but are thinner than the distal segments of the awns of primitive sheep. The wool undercoat fibers have thickened. Both fiber types are elongated and spiraled (FIGURE 19). The adult Merino sheep, the most efficient wool-producing sheep, has a coat consisting of elongated, regularly crimped fibers of uniform diameters and lengths (FIGURE 20). An analysis of the coat of the Merino lamb is essential for the identification of the types of fibers that form the coat of the adult sheep. The Merino lamb coat has bristle, awn, and wool fibers (FIGURE 21). During ontogeny, the bristles are shed and then replaced by wool fibers. The awn fibers lose their distal thickened segments, but the thin proximal segments persist. The wool fibers are retained, but are coarser than the wool of primitive sheep. Hence, the adult Merino sheep coat consists of wool fibers differ- entiating from follicles which produced kemp in the lamb, of awns deprived of their distal segments, and of wool fibers differentiating from follicles which produced wool in the lamb. A major difference between the Merino sheep and other sheep is in the nature of the hair follicles. Whereas the coat of other breeds is shed periodically and then new hairs differentiate from the follicles, the fibers of the adult Merino sheep grow from persistent germs and are not shed. In the evolution of the sheep coat from primitive wild sheep to the various domestic breeds, several changes have occurred. As summarized by Duer- den (1927), the domestic wooled sheep has evolved in the direction of the 151 Noback: Morphology and Phylogeny 489 loss of the protective coat both of bristles (kemp) and awns (heterotypes), the increase in length, density, and uniformity of the fibers, and the tend- ency of the retained bristles to become finer but still capable of being shed. In addition, the Merino sheep has developed persistently growing hair follicles. Important implications of the evolution of the sheep coat are that the types of hair in the hair coat may differ (1) in closely related animals and (2) at various stages of ontogeny with the same animal. Hence, data derived from a study of the coat of one animal species may not always apply to another animal species. Bibliography American Society for Testing Materials. 1948. Standards on textile materials. By the Society for Testing Materials. 560 pp. Philadelphia. BacCHRACH, M. 1946. Fur. 672 pp. Prentice-Hall. New York. BoLuicer, A. & M. H. 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Abt. Anat. u. Ontog. 55: 555-602. Mercer, F. H. 1942. Some experiments on the structure and behavior of the cortical cells of wool fibers. J. Council Sc. Ind. Research 15: 221-227. Miuier, C. 1939. Ueber den Bau der koronalen Schiippchen des Sdugetierhaares. Zool. Anz. 126: 97-107. Pax, F. & W. Arnpt. 1929-1938. Die Rohstoffe des Tierreichs. 2235 pp. Gebriider Borntraeger, Berlin. Sections in this reference are: FROLICH, G., W. SPOTTEL, & E. TAnzer. 1932. Haare und Borsten der Haussdugetiere. 1: 995-1221; Merse, W. 1933. Menschenhaar. 1: 1312-1363; ScHLtotr, M., E. Brass, W. STICHEL, & E. Kiumpp. 1930. Pelze. 1: 405-567; ScHLtott, M. 1933. Haare und Borsten von Wildsaugern. 1: 1222-1311. PFEIFER, E. 1929. Untersuchungen iiber das histologisch bedingte Zustandekommen der Lockung, mit besonderer Beriicksichtigung des Karakullammes. Biol. Generalis. 5: 239-264. Pinkus, F. 1927. Die normale Anatomy der Haut. In: Handbuch der Haut- und Geschlechtskrankheiten. 1: 1-378. J. Springer, Berlin. Pocock, R. 1914. On the facial vibrissae of mammalia. Proc. Zool. Soc. Lond. 40: 889-912. Rupatit, K. M. 1941. The structure of the hair cuticle. Proc. Leeds Philos. Soc. 4: 13-18: SmitH, H. H. 1933. The relationships of the medulla are cuticular scales of the hair shafts of the Soricidae. J. Morph. 55: 137-149. SmituH, S.& J. GLatsTeR. 1939. Recent Advances in Forensic Medicine. 264 pp. P. Blakiston’s Sons and Co. Phila. SPENCER, B. & G. SWEET. 1899. The structure and development of the hairs of mono- tremes and marsupials. Part 1. Monotremes. Quart. J. Micro. Sci. (N. S.) 41: 549-588. Stoves, J. L. 1942. The histology of mammalian hair. Analyst 67: 385-387. Stoves, J. L. 1943a. The biological significance of mammalian hair. Proc. Leeds Phil. and Literary Soc. 4: 84-86. Stoves, J. L. 19430. Structure of keratin fibres. Nature 151: 304-305. Stoves, J. L. 1944a. The appearance in the cross sections of the hairs of some car- nivores and rodents. Proc. Roy. Soc. Edinburgh 62B: 99-104. 153 Noback: Morphology and Phylogeny 49] Stoves, J. L. 1944b. A note on the hair of the South American opossum (Didel plis caranophaga). Proc. Leeds Philos. Soc. 4: 182-183. Stoves, J. L. 1945. Histochemical studies of keratin fibres. Proc. Roy. Soc. Edin- burgh. 62: 132-136. TAnzer, E. 1926. Haut und Haar beim Karakul im rassenanalytischem Vergleich. Halle a.d.S. (cited by: Pfeifer, 1929). Totpt, K., Jr. 1910. Uber eine beachtenswerte Haarsorte und iiber das Haarformen- system der Sdugetiere. Annalen d. K. K. Naturhistorischen Hofmuseums in Wien. 24: 195-265. Toxpt, K., Jr. 1912. Betrige zur Kenntnis der Behaarung der Sadugetiere. Zool. Jahrb. Abt. Syst. 33: 9-86. Totpt, K., Jr. 1935. Aufbau und natiirliche Farbung des Haarkleides der Wildsduge- tiere. 291 pp. Deutsche Gesellschaft fur Kleintier- und Pelztierzucht. Leipsig. Trotrer, M. 1932. The hair. Special Cytology (Cowdry, E. ed.) 1: 39-65. P. Hoeber. New York. VonBERGEN, W. & W. Krauss. 1942. Textile fiber atlas. Amer. Wool Handbook Co. New York. Witpman, A. B. 1932. Coat and fibre development of some british sheep. Proc. Zool. Soc. London 1: 257-285. Witpman, A. B. 1937. Non-specificity of the trio follicles in the Merino. Nature, Lond. 140: 891-2. Witpman, A. B. 1940. Animal fibres of industrial importance: their origin and identi- fication. 28 pp. Wool Industries Research Assoc. Torridon, Headingley, Leeds. Witpman, A. B. & H. Carter. 1939. Fibre-follicle terminology in the mammalia. Nature 144: 783-784. Wittrams, C. 1938. Aids to the identification of mole and shrew hairs with general comments on hair structure and hair determination. J. Wildlife Management 2: 239-250. Wynkoop, E.M. 1929. A study of the age correlations of the cuticular scales, medullae and shaft diameters of human head-hair. Am. J. Phys. Anthrop. 13: 177-188. Discussion of the Paper Docror M. H. Harpy (McMaster Laboratory, Glebe, NV. S. W., Austra- lia): 1 am glad Dr. Noback mentioned sheep, because the study of the ar- rangement of follicles in groups on these animals has disclosed some im- portant principles. Terentjeva,! Duerden,? and Carter® showed that de Meijere’s trio group is the basic unit in the follicle population of sheep. The trio (primary) follicles develop first and have accessory structures (sudoriferous gland, arrector pili muscle) which are absent from the later developing (secondary) follicles of the group.’ In the young lamb, it is the primary follicles which produce the coarse, and frequently medullated, kemp fibers and the secondary follicles which produce the fine and usually non-medullated wool fibers. These correspond respectively to the ‘over- hair’ and ‘underhair’ in Danforth’s classification. The primary follicles may produce kemp in the lamb and wool in the adult sheep, as Dr. Noback has mentioned. The size of the follicle groups, 7.e., the number of secondary follicles to each trio of primary follicles, varies greatly between breeds‘ and individuals® and also between body regions. The breeds and, to some extent, indi- viduals with the largest group size have also the greatest number of fibers to the square inch and the greatest uniformity of fiber thickness and length.° In the midside region, at least, the potential group size (including second- ary follicle rudiments in the young lamb) is strongly inherited, but the actual group size (number of active follicles) in the mature animal varies 154 492, Annals New York Academy of Sciences according to the food intake in the first year of life.’ Thus, it is possible to alter the group size experimentally. Varying the food intake in the second and third year of life had no marked effect on group size.3:9 It seems that many properties of the coat of the sheep depend on the inherited follicle group pattern and the modifications of this superimposed by the environment. Perhaps the same principles apply to other mammals. 1, 2: 3 TERENTJEVA, A. A. 1939. Pre-natal development of the coat of some fine-wooled breeds of sheep. C.R. Acad. Sci. U.R.S.S. (N.S.) 25: 557. DUERDEN, J. E. 1939. The arrangement of fibre follicles in some mammals, with special reference to the Ovidae. Trans. Roy. Soc. Edin. 59: 763. CarTER, H. B. 1943. Studies in the biclogy of the skin and fleece of sheep. 1. The development and general histology of the follicle group in the skin of the Merino. Coun. Sci. Ind. Res. (Aust.) Bull. 164: 7. . CarTER, H. B. & P. Davipson. Unpublished data. . CarTER, H. B. 1942. ‘‘Density’’ and some related characters of the fleece in the Australian Merino. J. Coun. Sci. Ind. Res. (Aust.) 15: 217. . CarTER, H. B. & M.H. Harpy. 1947. Studies in the biology of the skin and fleece of sheep. 4. The hair follicle group and its topographical variations in the skin of the Merino foetus. Coun. Sci. Ind. Res. (Aust.) Bull. 215: 5. . CarTER, H. B., H. R. Marston, & A. W. PErrRcE. Unpublished data. . Fercuson, K.A.,H.B. Carter & M.H. Harpy. 1949. Studies of comparative fleece growth in sheep. Aust. J. Sci. Res. B 2: 42. . Fercuson, K. A., H. B. Carter, M. H. Harpy, & H. N. TurNER. Unpublished data. 155 MOTIONS OF THE RUNNING CHEETAH AND HORSE By Mr_ton HitpEBRAND The horse is perhaps the most efficient running machine ever evolved; probably no other vertebrate has so many structural adaptations for rapid and untiring progress on the ground. The cheetah is conceded to be the fastest of all animals for a short dash, but lacks the endurance of the horse. This paper will analyze and contrast the running motions of these champions, and will reveal some of the secrets of the cheetah’s superlative speed. Several authors have noted cursorial adaptations of the cheetah (e.g., Pocock, 1927; Hopwood, 1947) but to my knowledge none has contrasted its mode of running with that of other cursorial quadrupeds. Morphological adaptations of the horse have been described by Howell (1944), Eaton (1944), Smith and Savage (1956) and many others. Those references emphasized structure; this paper stresses function. The classical study by Muybridge (1899) has remained the most important analysis of the motion of the horse. A paper by Grogan (1951) provides a concise review of the sequence of footfalls and combinations of supporting members. MATERIALS AND METHODS This study was inspired by the excellent film sequence of a running cheetah in the Walt Disney True Life Adventure picture “African Lion.” I am grateful to Walt Disney Productions for furnishing film strips for analysis. The photographer, Alfred Malotte, filmed the animal with a telephoto lens, so perspective changes slowly during the run. The chase presented is actually a combination of two dashes: a slower, shorter one, filmed at regular speed, and one taken in slow motion. Sequences of three and seven consecutive strides show the cheetah about side-on to the camera. With a Recordak Film Reader, 155 successive frames were traced. Registration points permitted these to be redrawn as a composite picture, with the images in proper spatial relationship to one another. The film outlines are not sharp, and low vegetation usually obscured the feet when they were on the ground, but there are enough nearly identical frames to establish a ground line and a reasonably accurate depiction of motions. The analysis for the horse was made from photographs in Muybridge (1899: 48] 156 482 JOURNAL OF MAMMALOGY Vol. 40, No. 4 171-179) and from the film “Horse Gaits,” produced by the Horse Association of America, Inc. In the latter, action was filmed with an electric camera at 128 frames per second; the sequence analyzed shows the horse “Citation” winning the mile-and-one-quarter American Derby in 1948. The method of analysis was the same as with the cheetah. FINDINGS Speed.—Figure 1 shows speed records of the horse and, for comparison, of man, for distances up to 900 yards, expressed as rate of travel and lapsed time. Approximate speed of the cheetah is also indicated. The maximum measured speed for man is 22.28 mph, over 220 yds.; the plotted curve shows that he could average 22.6 mph for 155 yds. The horse has run %4 mi. at 43.27 mph; it could probably average 44 mph for 300 yds. The speed of the cheetah is legendary, yet scantily documented. Authors quote each other and the estimates of lay observers. However, there is both direct and indirect evidence of great speed. Because many artiodactyls will run parallel to a moving vehicle, accurate data are available on the speed of some of them. Einarsen (1948) reported that the pronghorn normally can run at 50 mph, and under favorable conditions can attain 60 mph. On a California desert a pet cheetah overtook a young buck pronghorn (Mannix, 1949). Craighead (1942) stated that the cheetah often runs down its quarry within 150 yds., and that it is not unusual for a cheetah to overtake an antelope that has had a head start of 100 yds. or more. At Ocala, Florida, John Hamlet includes a cheetah in an animal show fea- turing species employed in hunting. The cheetah is trained to run in a long enclosure. A popular article (Severin, 1957) reported the results of a speed test stating that “from a deep crouch Okala spurted to the end of the 80 yard course in 24 seconds, for an average speed of about 71 miles an hour.” Unfor- tunately, this record must be disregarded because the enclosure is, in fact, about 65 yards long, the method of timing was inexact, and there is an arith- metical error. It is a general consensus that this remarkable cat can run at least 70 mph. The speed of the cheetah in the film strips analyzed in this paper could be computed if the film speeds and the animal’s body length were exactly known, but these can only be approximated. The studio reported film speeds of about 24 and 48 frames per second; efforts to check these figures with the photographer were unsuccessful. The animal shown is a male. Male cheetahs average about 7 ft. in length (records taken from Hollister, 1918; Shortridge, 1934; Bryden, 1936; Roberts, 1951); the largest of record measured 7 ft. 9 in. Separate cal- culations based on assumed animal lengths of 6% and 7% ft., and (for the slow- motion sequence ) on film speeds of 46 and 50 frames per second give a range of possible speeds between 37% and 49 mph. Since the animal had to find 157 Nov., 1959 HILDEBRAND—MOTIONS OF CHEETAH AND HORSE 483 its footing among scattered shrubs that were 6 to 24 in. high, these less-than- optimum speeds seem expectable. Endurance.—Records of animal endurance that are accurate and compar- able are difficult to secure. Figure 2 presents some relatively reliable data. The human distance records were taken from various editions of The World Almanac. Records for the horse are from the same source and from Howell (1944), who also cited a record (dating from 1853) of 100 mi. at 11.2 mph. If accurate, this is truly remarkable: on the basis of curves plotted from other records one would expect no more than a 9-10 mph rate for this great distance. Andrews (1933) reported following another perissodactyl, the Mongolian wild ass (Equus hemionus), over open country with an automobile. One particular animal ran 16 mi. at an average speed of 30 mph “as well as could be estimated”; the next 4 mi. were covered at about 20 mph. It ran 29 mi. before it stopped from exhaustion. Since it repeatedly changed direction and speed, these figures must be taken as approximate, but it is unlikely that any other cheetah 7 ? 70 60 50 50 - =) fo) = i) 40 402 o 5 a. oO @ 7) ” @ =30 30 = 20 20 10 10 fe) fe) fe) 200 400 600 800 Yards fe) 1 2 3 4 Furlongs Fic. 1.—Speed records of the cheetah (approximate), horse and man, expressed as rate of travel (solid lines and left ordinate scale) and lapsed time (dashed lines and right ordinate scale). Source for man and horse: several editions of The World Almanac. 158 484 JOURNAL OF MAMMALOGY Vol. 40, No. 4 animal could equal this feat over distances greater than 3 mi. (The pronghorn is faster for short distances, according to Einarsen, 1948. ) In sharp contrast to the equids noted, the cheetah seldom runs more than % mi. Pocock (1927) claimed that 600 yds. is the maximum distance for a chase at speed, and Bryden (1936) stated that two mongrel dogs brought one to bay in 2% mi. Prey species are almost invariably overtaken by the cheetah, ° and usually knocked to the ground. However, if they can scramble to their feet and run again, the cheetah often abandons further pursuit. 60 Miles per hour fe) = fe) 10 20 30 40 50 Miles Fic. 2.—Endurance records of the pronghorn, Mongolian wild ass, race horse and man, expressed as average rate of travel for different distances. Sources cited in text. 159 Nov., 1959 HILDEBRAND—MOTIONS OF CHEETAH AND HORSE 485 The longer of the dashes on the film analyzed in this paper was about 325 yds. Sequence of footfalls——The leading front or hind foot is second of the pair to touch and leave the ground in each stride or cycle of movement. An un- qualified reference to lead applies to the front feet: an animal is said to be running with a left lead if the left forefoot is placed in front of its opposite. I will call the other member of each pair the trailing limb. In the extreme flexed position the galloping horse passes one hind foot forward of one forefoot (Fig. 4e). Since the legs have little lateral motion and nearly equal straddle, the animal can avoid interference only by a sequence in which the leading forefoot is followed with the hind foot on the other side of the body. Thus the front and back legs must use the same lead. This sequence of footfalls, diagrammed in Fig. 3, is termed the transverse gallop. In the extreme flexed position the cheetah passes both hind feet forward of both forefeet (Fig. 5h). To avoid interference it must therefore straddle the forelimbs with the hind limbs. It would seem that the lead of the fore- and hind limbs could be independent, but in practice the leading forefoot is followed by the hind foot on the same side—a sequence of footfalls called the rotary (or lateral) gallop. If the legs on one side of the body were extended as those on the other side were gathered together, and if the spine were flexed to right and left, then the rotary sequence of footfalls would increase the reach of the limbs slightly (about 2 inches per stride for a 7° swing of shoulders and pelvis with a straddle of 8 inches), but this is not the case. Perhaps the rotary sequence provides subtle benefits to balance or muscle function. The domestic cat commonly places the hind feet nearly opposite one another when running (a gait termed the half bound) but, curiously, it may on occasion follow the horse rather than the cheetah, using the transverse gallop (Muy- bridge, 1899). Left Hind Right_Hind igh isenorit ieee eee eens , one Horse stride Left Hind Right Hind =e Left Front Right Front ' Right Hind Se Rig Cheetah one stride 0) | 2 3 a Fic. 3.—Sequence of footfalls and phases of one representative stride, shown in relation to time in tenths of seconds. The period that each foot is on the ground is shown by the length of its respective line. 160 486 JOURNAL OF MAMMALOGY Vol. 40, No. 4 Phases of the stride and their duration—tThe galloping animal has all feet off the ground one or more times in each stride, and during periods of support the legs are used in different combinations. Each suspended period and each combination of supporting members is called a phase. There is much individual variation in the phases of gaits. Indeed, Howell (1944: 222) reported 16 different phase formulas for galloping horses. However, a usual phase formula can be selected for analysis. The nature and duration of the phases of such a formula of the galloping horse and cheetah are shown in Fig. 3. The horse has all feet off the ground once in each stride—in the flexed position (see Fig. 4e). Howell (1944: 240) depicted a light horse that had a second, brief suspended phase, just before the trailing forefoot struck the ground, but this is unusual. The cheetah is suspended when flexed, and again when extended. I believe there is sometimes a third, though fleeting, instant of suspension—between falls of the front feet (Fig. 3 and positions d, f and h, Fig. 5). Muybridge (1899: 157) anticipated this circumstance when he wrote, “It is probable that future research will discover—with the horse and some other animals—during extreme speed, an unsupported transit from one anterior foot to the other.” Analysis of Fig. 3 shows that the galloping horse characteristically has one suspended and seven supported phases (the supported transit from one fore- foot to the other being almost instantaneous when galloping at good speed). The cheetah has three suspended and five supported phases. The duration of each phase varies not only with speed but also with the Fic. 4.—Five positions of a galloping horse shown in correct spatial relationship. Trajec- tories followed by the front feet are indicated above, those by the hind feet below, long dashes for right feet and short dashes for left feet. Positions of footfalls are shown by spots on the ground line. Figures below ground line give for each interval its percentage of total stride distance. 161 Nov., 1959 HILDEBRAND—MOTIONS OF CHEETAH AND HORSE 487 individual and for the same individual at different times. The following statements are as representative as the material available permits, but are only approximations of any particular performance. When galloping at 35 mph the horse completes one stride in about .44 second, or 2% strides per sec.; at about 45 mph the cheetah completes one stride in about .39 second, or 2% strides per sec. The horse is supported during % of its stride and the cheetah during only half of its stride. Each animal is supported by two legs for 11 to 12 per cent of its total support period. The trailing hind foot of the horse is on the ground about 85 per cent as long as the leading hind foot, whereas the two hind feet of the cheetah are on the ground about the same amount. The disparity betwen the animals is greater for the forefeet: the trailing forefoot of the horse is on the ground 80 per cent as long as the leading foot, whereas with the cheetah the foot that has the shorter contact is the leading foot (about 95 per cent as long as that of the trailing foot). Change of lead.—These differences in duration of support and the asymmetry in resulting stresses require a change in lead from time to time to postpone fatigue. Further, a galloping animal can turn more sharply by leading with the inside forefoot. Unless rider or terrain demand frequent turning, a horse changes its lead most often to compensate for the relatively great discrepancy in the duration of support provided by leading and trailing legs. Actual lead reversal is usually accomplished first by the forelimbs, but the motion of the hind limbs must be coordinated to avoid the interference that would otherwise result. Probably the spacing of the footfalls must also be altered, and it is likely that average speed will be reduced slightly if the lead is changed frequently. The cheetah’s leading and trailing legs share the exertion of running more evenly, but sharp and frequent changes of direction are usually dictated by the evasive quarry. The cheetah in the film strip changed lead three times in a sequence of 33 strides, and nine times in a sequence of 34 strides. Only once was the same lead used consecutively more than seven times, and five times it was changed after three or fewer strides. Fic. 5.—Eight positions of a galloping cheetah, shown in correct spatial relationship. Sym- bols and figures as for Fig. 4. 162 488 JOURNAL OF MAMMALOGY Vol. 40, No. 4 Several factors contribute to the facility with which the cheetah changes lead, and it is unlikely that speed is sacrificed. In contrast to the horse, there is a time in the stride of the cheetah (just following position d, Fig. 5) when the two front and two hind feet are opposite one another in both the horizontal and vertical planes. At this instant the lead can be changed as quickly and smoothly as not, and since this position immediately precedes the placement of the first (trailing) forefoot, the animal need not long anticipate the change of lead required by a turn, and cannot easily be thrown off balance by the dodging of its prey. Length of stride ——The spacing of footfalls, and hence total length of stride, varies considerably with speed and individual performance. The data pre- sented here are indicative of usual distances. They are based on five strides of three horses and on ten strides of a cheetah. The strides of the galloping horse recorded by Muybridge (1899) varied from nearly 19 ft. to nearly 23 ft., and averaged 22.8 ft. Exceptional horses are reputed to cover 25 ft. at a stride (Howell, 1944: 241). Assuming the cheetah of the film strip to be 7 ft. long, the shortest of the seven strides traced was 21 ft., the longest 26 ft., and the average 23 ft. Thus the cheetah covers at least as much ground per stride as does the horse in spite of the great disparity in body sizes: the stride of the cheetah is 8% to 11% times its shoulder height (with supporting forelegs vertical), compared with 4% to 5 for the horse; or 5% to 64 times its chest-rump length (in position of maximum extension), compared with 3% to 4 for the horse. The cursorial skill of the cheetah results in large measure from its ability to achieve so long a stride. The number and duration of the suspended phases of its gait contribute; other factors are considered further in following sections of this paper. In Figs. 4 and 5 the footfalls are marked by dark spots on the ground lines. The per cent of total stride involved in each interval is indicated by the numbers below the ground lines. The most evident difference between the two animals in spacing of footfalls is the greater percentage of stride (51 against 30) that the cheetah achieves between the strike of the leading hind foot and that of the trailing forefoot. At this time it is bounding forward with all feet off the ground; at a corresponding time the horse is supported (compare Figs. 4b, and 5d). If we arbitrarily eliminate the difference by reducing this par- ticular interval of the cheetah’s stride to 30 per cent of total stride (as with the horse) and adjust the remaining three percentages accordingly (making the sum of the intervals again 100 per cent), the horse still has a slightly longer reach between the two hind feet and covers less ground in its suspended transit from leading front foot to trailing hind foot. Support role of the forelegs.—It has been said that the front legs of a galloping horse do nothing that a wheel would not do better. To be strictly true, the wheel would need to be versatile at banking and at shifting track to maintain the balance of its load, yet support is certainly the principal function of the 163 Nov., 1959 HILDEBRAND—MOTIONS OF CHEETAH AND HORSE 489 equid forelimbs. The hind quarters are closest to the ground when the hind feet are on the ground (see croup-to-ground curve, Fig. 7), but the withers, in contrast, start to rise when the first (trailing) front foot strikes the ground and continue to rise until the leading front foot is lifted. The cushioning of body impact by the digital ligaments (Camp and Smith, 1942) and the muscles that suspend the thorax between the shoulder blades does not prevent the forequarters from rising as they pass over the stiff front legs which are pivoting on the supporting feet. The variation in withers-to-ground height is only 1% to 2 inches, about one-third of the variation in croup-to-ground height. It is not possible to determine the deceleration of forward motion that results from the lift given the body by the front legs, but, making some reasonable assumptions, we can learn its order of magnitude. If a 1150-Ib. horse galloping 40 mph lifts half of its weight 2 inches as the stiff forelegs pivot forward over the supporting feet, the resulting deceleration will be .034 mph. Conclusion: in regard to speed, a wheel would do nothing for a horse that its front legs don’t do just about as well. Figure 7 shows that the shoulders of the cheetah are falling when the trailing forefoot strikes, continue to fall all the time the front feet are on the ground, and start to rise again only as the first hind foot strikes the ground. Evidently the front legs provide little support and no deceleration, yet, before concluding that the cheetah could run without wheel or forelegs, we must consider other functions of its front legs. Role of the back.—Like other carnivores the cheetah sharply flexes and extends the spine when running. For reasons considered in the next section, the heavy-bodied horse must hold its back nearly rigid, although there is some motion at the sacrum. The amounts of flexion and extension for the two animals, approximated from photographs, are shown in Fig. 6. The angle that the pelvis makes with the scapula changes about 60° in the running horse, and about 130° in the running cheetah. The rotation of the scapula on the spine is about the same (roughly 20°) in each animal, so the 70° difference between them is attributable to the spine. In both animals the motion of the spine in the vertical plane is greater at the pelvis than at the shoulder. Of what advantage is a supple spine to a cursorial animal? One would expect flexion and extension of the spine to increase the swing of the limbs, thus increasing the distances covered during the suspension phases of the stride and extending the duration of the support phases. If this is true, the angles between ground line and limbs as they strike and leave the ground should be more acute for the cheetah than for the horse. The instant of impact of the feet is difficult to determine from the somewhat blurred images of the available moving-picture frames, so I cannot offer quanti- tative data, but it appears that these angles are indeed more acute for the cheetah. Swing of the limbs is accomplished for the horse almost exclusively by muscles inserted on the limbs, while muscles of the back also contribute for the 164 490 JOURNAL OF MAMMALOGY Vol. 40, No. 4 cheetah. This is of significance. If two muscles move one bone on another, the force of rotation is equal to the sum of the individual forces whereas the velocity is limited to that of one muscle acting alone (assuming comparable and adequate leverages and intrinsic rates of contraction). However, if a muscle moves one bone on a second while another muscle moves the second bone in the same direction on a third bone, then there is summation of both force and velocity. Thus, on the recovery stroke, the swing of a limb can be hastened by flexing several of its joints. (Shortening the limb also decreases the load on the muscles. ) But when a limb is supporting the body, only a limited amount of motion is possible between the limb joints. Therefore, by swinging its limbs with two independent sets of muscles (of the limbs and of the back) the cheetah increases the speed of its stride. Although the forward extension of the limbs when the feet strike the ground is only a little greater for the cheetah than for the horse, the more supple spine of the former contributes to substantially greater maximum forward extension before the feet start their backward acceleration preliminary to striking the ground (Fig. 6). Further, comparing the trajectories traced by the feet, as shown in Figs. 4 and 5, it is clear that, in the position of maximum forward extension, the limbs of the cheetah are held higher than are those of the horse. Indeed, they are not only higher relative to body size, but actually higher by about one-third for the front feet and trailing hind foot. It follows that the feet of the cheetah travel farther in moving to the ground. It may be inferred that they have greater backward acceleration when they strike the Fic. 6.—The galloping horse and cheetah, shown in positions of maximum flexion and extension of the spine and maximum rotation of the scapula on the spine. 165 Nov., 1959 HILDEBRAND—MOTIONS OF CHEETAH AND HORSE 491 ground and that they probably develop enough traction to prevent any decelera- tion from factors discussed below and in the next section. In the flexed position the chest-buttock length of the horse is 80-90 per cent of its length in the extended position (87 in my analysis; 81 in an instance reported by Howell, 1944: 240). The flexed length of the cheetah is only about 67 per cent of its extended length. The actual shortening of the body accom- plished by flexion is about 16 in. for the cheetah and 9 in. for the horse. In Fig. 7, changes in chest-buttock length are synchronized with duration of contact of each foot with the ground. For the cheetah, flexion from the position of maximum body length (high points on upper curve) is initiated when the body is unsupported. This helps impart backward acceleration to the front foot that is about to strike the ground. However, any considerable body flexion at this time would tip the shoulders forward and reduce the reach of the leading front leg, so sharp flexion is postponed to the instant the leading foot strikes. Flexion is then rapid, and is nearly completed while that foot is on the ground; only a little more body shortening is accomplished as the leading front foot follows through. Thus the fore- and hindquarters are not significantly drawn toward one another by flexion of the spine: the hindquarters alone move toward the forequarters as the latter are fixed by the forelegs (with reference to the ground, their deceleration is prevented). In similar manner, extension of the body starts as the trailing hind foot initiates its down stroke. Again this action must help give that foot acceleration to the rear. Some extension also accompanies the unsupported follow-through of the hind legs, but most of the body extension occurs when the hind feet are on the ground. Since backward motion (deceleration) of the hindquarters is thus prevented by the hind legs, nearly all of the increase in body length re- sulting from extension is added to the length of the stride. We see that the body of the cheetah moves forward like that of the measuring worm. The added distance is nearly 15 in. per stride, giving an increment in speed of 2 to 2% mph at a rate of about 40 mph. What the increment might be at greater speeds will depend on the relative roles played by increased length of stride and increased rate of stride as the animal moves faster. It seems probable that at 60 mph the animal adds in this manner at least 3 mph to its rate of travel. A limber spine contributes to speed in still another way. As the cheetah’s trailing foreleg strikes the ground, its forequarters and hindquarters are moving with equal velocity. But while the front feet are on the ground, the body is flexed on the forelimbs so that, at the instant the leading foot leaves the ground, the hindquarters have greater forward velocity than the forequarters. (The energy necessary to bring this about is here considered to be exerted by muscles of the back and forelimbs, against the ground as traction.) The difference between the velocity of the shoulders and of the center of mass of the entire body is nearly 3% ft. per sec. when the animal is running at 45 mph. (The fig- ure was derived by estimating the positions of the respective points on tracings 166 492, JOURNAL OF MAMMALOGY Vol. 40, No. 4 of the animal plotted from successive moving-picture frames and then measur- ing their relative motion in a known time interval.) In other words, when the forelimbs are on the ground, the portion of the body to which they are joined is moving forward nearly 2% mph. slower than the body as a whole. Similarly, when the hind feet are on the ground the pelvis is also moving slower than the body as a whole. It is reasonable to surmise that speed is benefited by this circumstance, for it reduces the backward velocity (though not the force ) required of the legs in order to propel the body forward. Body size, speed and endurance.—The speed at which an animal can run is a function of length and duration of stride. Each of these factors is related to body size. If it were possible to disregard mass, then animals of like form would run at the same speed regardless of body size, because length of stride varies in direct proportion to linear measure whereas intrinsic rate of muscle contraction, and hence rate of stride, varies inversely with linear measure ( Hill, 1950). It is true that the red fox can run as fast as a horse although it is one-tenth as long, but mass cannot be neglected: the horse weighs 100 times as much as the fox, and with like form could scarcely run at all. The force of contraction of a muscle is proportional to the cross-sectional area of its fibers, therefore varying as the square of linear measure. The mass of the body varies as the cube of linear measure, so largeness places the muscles at a disadvantage even when the body is at rest. In motion the disadvantage is greater (Hill, op. cit.) because as body size increases the power the muscles can deliver does not quite keep up with the demands placed on them to control the kinetic energy devel- oped in oscillating parts of the body. To avoid impossible stresses, a large animal must therefore modify the form and function of its body to reduce the load placed on its muscles and supportive tissues. Since momentum is the product of mass and velocity, this can be done by minimizing the motion of one part of the body relative to another, by causing its center of mass to move in as nearly a rectilinear fashion as possible, and by reducing the mass of such structures as must change their velocities. These principles, and related structural adaptations, are noted in publications cited above and in the introduction to this paper. To run at all, the horse must have a degree of efficiency that assures both speed and endurance. The fox has both speed and endurance for a different reason: its mass is so small that inertia does not increase sufficiently with speed to cause distress. What of the cheetah? At 125 lbs. the cheetah is only about one-ninth as heavy as the horse, but it is about 14 times as heavy as the fox. Miohippus, some litopterns, and many artiodactyls are (or were) of comparable size, but have cursorial mechanisms that conserve energy more effectively than does that of the cheetah. Why is not this cat either smaller or more like the horse in the form of its body and the way that it runs? The answer is that the cheetah does not need to be efficient; it needs to be 167 Nov., 1959 HILDEBRAND—MOTIONS OF CHEETAH AND HORSE 493 fast, and its size is about optimum for maximum speed. Its muscles can stand the strain long enough for the animal to run the necessary 400 to 600 yds., so greater efficiency is not needed. However, if its body were heavier, then even for such short distances it could not employ every mechanism for gaining speed while disregarding those that improve efficiency. Its speed, then, imposes an upper limit on its body size. There are probably several reasons why the cheetah is not smaller: its size gives it wide vision, independence of irregu- larities in the terrain, and enough weight to bring down its prey. SUMMARY The cheetah is the fastest of animals for a short dash, and the horse has superlative endurance. These animals differ greatly in body size, so it is instructive to compare their ways of running. Analysis was made from slow-motion moving-picture sequences by tracing images of successive frames and arranging them in correct spatial relation to one another. The cheetah can sprint at 70 to 75 mph; the horse can attain 44 mph for 300 yds. The cheetah seldom runs more than 4 mi., the horse can run at 20.5 mph for 20 mi., and its rate ee ee ae ee ir length croup to ground withers to ground chest-buttock length shoulder to ground ” tail-base to ground Cheetah Fic. 7.—Relation of body movement to action of the feet during a little more than four strides. Motion is from left to right. Lower broken lines show, in the manner of Fig. 3, the periods of contact of the feet with the ground; letters R, L, H and F mean right, left, hind and front, respectively. Upper curves indicate, by distance above the base lines, variation in chest—buttock length. Middle curves depict height of shoulders (withers) and tail base (or croup) above the ground. All distances above the base line are in proportion to maximum chest—buttock length, which is equated for the two animals. 168 494 JOURNAL OF MAMMALOGY Vol. 40, No. 4 of travel declines only slowly as distances increase over 30 mi. The endurance of the Mon- golian wild ass is apparently superior to that of the horse. The horse uses the transverse gallop, usually covers 19 to 25 ft. per stride and completes about 2% strides per sec. at 35 mph. Its body is suspended once in each stride, during one-quarter of the stride interval. The leading front and trailing hind limbs support the body longer than their opposites. A change of lead usually occurs first for the front feet, but must be anticipated well before the trailing front foot strikes the ground. The forward motion of the front limbs as they pivot on the supporting feet raises the forequarters, but the resulting deceleration of the body is negligible. Its mass and inertia require that the horse minimize the motion of one part of the body relative to another and move its center of mass in a nearly rectilinear fashion: the feet are not lifted high, there is little up-and-down motion of withers and croup, and the back is relatively rigid. The cheetah uses the rotary gallop, covers as much ground per stride as the horse, and at 45 mph completes about 2% strides per sec. The body has two long periods of suspension (and probably a short one) in each stride, adding up to half of the stride. The trailing front foot is on the ground a little longer than the leading foot; the two hind feet have about equal periods of support. Changes of lead are smoothly accompilshed, and can be initiated an instant before the trailing front foot strikes the ground. The front limbs do not raise the forequarters. Body size is about optimum for maximum speed: it is small enough so body form and motion can be adapted for speed with little regard for efficiency, yet large enough to gain a long and rapid stride, as noted below. The feet are lifted high. There is pronounced up-and-down motion of shoulders and pelvis, and marked flexion and extension of the spine. Flexion and extension of the back contribute to speed by: (1) increasing the swing of the limbs, thus increasing the distance covered during suspended phases of the stride and increas- ing the duration of the supported phases; (2) advancing the limbs more rapidly, since two independent groups of muscles (spine muscles and intrinsic limb muscles) acting simul- taneously can move the limbs faster than one group acting alone; (3) contributing to increased maximum forward extension of the limbs, which permits their greater backward acceleration before they strike the ground; (4) moving the body forward in measuring-worm fashion; and (5) reducing the relative forward velocity of the girdles when their respective limbs are propelling the body. Speed is the product of stride rate times length. Relative to shoulder height, the length of the cheetah’s stride is about twice that of the horse. Factors contributing to its longer stride are: (1) two principal suspension periods per stride instead of one; (2) greater proportion of suspension in total stride; (3) greater swing of limbs, so they strike and leave the ground at more acute angles; and (4) flexion and extension of the spine synchronized with action of the limbs so as to produce progression by a measuring-worm motion of the body. The rate of the cheetah’s stride is faster than that of the horse because: (1) its smaller muscles have faster inherent rates of contraction; (2) its limbs are moved simultaneously by independent groups of muscles; (3) its feet move farther after starting their down strokes before striking the ground, thus developing greater backward acceleration; (4) the fore- limbs have a negligible support role and probably actively draw the body forward; (5) the limbs are flexed more during their recovery strokes; and (6) the shoulders and pelvis move forward slower than other parts of the body at the times that their respective limbs are propelling the body. LITERATURE CITED AnprEws, R. C. 1933. The Mongolian wild ass. Nat. Hist., 33: 3-16. Brypen, H. A. 1936. Wild life in South Africa. Geo. G. Harrap & Co., Ltd., London. pp. 282. Camp, C. L. anp Natrasua SMitH. 1942. Phylogeny and functions of the digital ligaments of the horse. Memoirs Univ. Calif., 13 (2): 69-124. 169 Nov., 1959 HILDEBRAND—MOTIONS OF CHEETAH AND HORSE 495 CRAIGHEAD, JOHN AND FRANK. 1942. Life with an Indian prince. Nat. Geogr. Mag., 81: 235-272. Eaton, T. H., Jr. 1944. Modifications of the shoulder girdle related to reach and stride in mammals. Jour. Morph., 75 (1): 167-171. ErnarsENn, A. S. 1948. The pronghorn antelope. Wildlife Management Inst., Wash. D. C. pp. 238. Grocan, J. W. 1951. The gaits of horses. Jour. Amer. Vet. Med. Assn., 119 (893): 112- 117. Hm, A. V. 1950. The dimensions of animals and their muscular dynamics. Science Progress, 38 (150): 209-230. Ho.utster, Nep. 1918. East African mammals in the United States National Museum. Bull. U.S. Nat. Mus., 99, Pt. 1. Horwoop, A. T. 1947. Contribution to the study of some African mammals. III, Adapta- tions in the bones of the fore-limb of the lion, leopard, and cheetah. Jour. Linn. Soc. (Zool.), 41: 259-271. Howe, A. B. 1944. Speed in animals. Univ. Chicago Press. pp. 270. MANNIX, JULE. 1949. We live with a cheetah. Sat. Evening Post, 221 (37): 24 ff. MuysripcE, Eapwearp. 1899. Animals in motion. Chapman & Hall, Ltd., London, pp. 264. [Republished with minor changes, 1957. Ed. by L. S. Brown. Dover Publ., Inc. pp. 74, 183 pls. References in present paper are to 1899 ed.] Pocock, R.I. 1927. Description of a new species of cheetah (Acinonyx). Proc. Zool. Soc. London, 1927: 245-252. Roserts, Austin. 1951. The mammals of South Africa. Contr. News Agency So. Africa, pp. 700. SEVERIN, Kurt. 1957. Speed demon. Outdoor Life, 119 (4): 54 ff. SuHortTRipcE, G. C. 1934. The mammals of Southwest Africa, vol. I. W. Heinemann, Ltd., London. pp. 437. SmitH, J. M. AnD R. J. G. Savace. 1956. Some locomotory adaptations in mammals. Jour. Linn. Soc. (Zool. ), 42 (288): 603-622. Dept. of Zoology, Univ. of California, Davis. Received March 28, 1958. ADDENDA The last paragraph on p. 482 notes that estimates of speed for the cheetah studied were based on information from Disney Studios that the film analyzed was made at 48 frames per second. The photographer, Alfred Malotte, could not be reached when the paper went to press, but now informs me that the film speed was 64 frames per second. This increases my estimate of the animal’s speed to 56 mph and the rate of the stride (top page 487 and Fig. 3) to one stride in .28 seconds or about 3% strides per second. On p. 491 it is stated that the cheetah adds about 15 inches to each stride by a meas- uring worm motion of the back. This should have been 15 inches two times per stride (when the back is flexed and again when it is extended), and, with the revised estimate of stride rate, the benefit to speed becomes about 6 mph. 170 NATURAL HISTORY MISCELLANEA Published by The Chicago Academy of Sciences Lincoln Park - 2001 N. Clark St., Chicago 14, Illinois No. 170 October 30, 1959 Toxic Salivary Glands in the Primitive Insectivore Solenodon GEORGE B. RABB* In 1942 O. P. Pearson demonstrated the toxic property of the saliva of Blarina brevicauda, a common shrew of the eastern United States, and identified its principal source as the submaxillary gland. Compara- tive studies at that time and subsequently revealed that similar poison- ous factors were not present in the salivary glands of other soricid and talpid insectivores (Pearson, 1942, 1950, 1956). I had an unexpected opportunity to make a crude check on the salivary glands of Solenodon paradoxus, a remote relative of the shrews, when three of these animals died at the Chicago Zoological Park within two months after their arrival in 1958 from the Dominican Republic. Parts of the submaxillary and parotid glands of one animal that had died one to two hours beforehand were ground separately with sand, diluted to 10 per cent by weight solutions with 0.9 per cent NaCl solution, and filtered, following the procedure of Pearson (1942). These solutions were injected into a small series of male white mice that ranged in weight from 29 to 44 grams. All of the mice injected with extract from submaxillary gland showed some reaction — at least urination and irregular or rapid breathing for several minutes. Five that received intravenous doses of extract of .09 to .38 mg. submaxillary gland per gram of body weight did little more than this and recovered within 30 minutes. Five that received intravenous doses of .38 to .55 mg. per gram additionally ex- hibited protruding eyes, gasping, and convulsions before dying within two to six minutes. Two animals that had intraperitoneal injections of extract of .56 and .66 mg. per gram died in about 12 hours, and one injected at the level of 1.02 mg. per gram died in 13 minutes. Urination, cyanosis, and depression were observed in these animals. Three ‘‘con- trol” mice injected intravenously with extract of 1.02, 1.68, and 1.87 *Chicago Zoological Park, Brookfield, Illinois 171 No. 170 The Chicago Academy of Sciences, Natural History Miscellanea mg. of parotid gland per gram of body weight showed no distress except for initially very rapid breathing in the last case. In general these results are very like those described for Blarina extracts. It may be noted that the twentyfold lesser potency evident here of Solenodon extract as compared to that of Blarina may be due to postmortem inactivation of the toxic principle as reported by Eils and Krayer (1955) for fresh Blarina material. Further tests with the refined techniques of these authors using acetone treated glands will be necessary for a fairer assessment of the potency of Solenodon toxin. Sections were made of the submaxillary glands and stained w.th hematoxylin and eosin and also with a modification of Mallory’s tr.ple stain. These sections showed some large cells with coarse acidophilic granules and small nuclei in the secretory ducts. Pearson (1950) sus- pected that such cells in Blarina might be concerned in the production of the saliva’s toxic principle, although somewhat similar cells are found in other soricids. The submaxillary glands of Solenodon are rather enormous and con- spicuous structures (see fig. 47 in Mohr, 1938). Each gland weighs three to four grams in adult animals. According to Allen (1910), the duct of the submaxillary gland ends at the base of the large deeply channeled second incisor tooth of the lower jaw (see fig. 19D in Mc- Dowell, 1958). Presumably toxic saliva would be conducted thereby into a wound. I could not induce Solenodon to bite live mice and there- fore have no direct evidence on this point. However, in 1877 Gundlach reported inflammatory effects of bites by Cuban Solenodon to himself and a mountaineer (although he dismissed the possibility of venomous action on the basis of authority!). Of his hand bite he said: “... I was bitten by the tame individual, which gave me four wounds cor- responding to the [large] incisors: those from the two upper incisors healed well, but those from the lower ones inflamed.” Moreover, there are indications that Solenodon is not immune to its own venom. Autopsy of the third animal disclosed multiple bite wounds on the feet and no obvious internal evidence of other causes of death. Sections of the liver show considerable congestion in that organ. The snout, lips, limbs, and tail were very pale the afternoon preceding death. Mohr (1937, 1938) gave accounts of several cases in which death was the outcome of fighting with cage mates although only slight foot wounds were inflicted. Pearson (1950) reported that Blarina was rela- tively immune to its own venom, although the single test animal died and the interpretation was problematical. The utility of the venom for 172 Rabb: Toxic Salivary Glands of Solenodon 1959 Solenodon in its natural environment is unknown and is certainly not indicated by its insectivorous habits. The explanation may be phylo- genetic and historical rather than one of present-day function. I wish to acknowledge the help of the park’s veterinarian, W. M. Williamson, and medical technician, Ruth M. Getty. Literature Cited Allen, Glover M. 1910. Solenodon paradoxus. Mem. Mus. Comp. Zool., 40: 1-54. Ellis, Sydney and Otto Krayer 1955. Properties of a toxin from the salivary gland of the shrew, Blarina brevicauda. Jour. Pharmacol. and Exptl. Therap., 114: 127-37. Gundlach, Juan 1877. Contribucion a la mamalogia Cubana. Havana, G. Monteil, 53 pp. McDowell, Samuel B., Jr. 1958. The Greater Antillean insectivores. Bull. American Mus. Nat Bist..91 153) 7113-214, Mohr, Erna 1937. Biologische beobachtungen an Solenodon paradoxus Brandt in Gefangenschaft. III. Zool. Anz., 117: 233-41. 1938. Biologische beobachtungen an Solenodon paradoxus Brandt in Gefangenschaft. IV. Ibid., 122: 132-43. Pearson, Oliver P. 1942. On the cause and nature of a poisonous action produced by the bite of a shrew (Blarina brevicauda). Jour. Mamm., 23: 159-66. 1950. The submaxillary glands of shrews. Anat. Record, 107: 161-69. 1956. A toxic substance from the salivary glands of a mammal (short-tailed shrew). pp. 55-58 in Venoms, ed. E. E. Buckley and N. Porges, American Assoc. Adv. Science Publ. No. 44, xii + 467 pp. 173 Altitudinal Zonation of Chipmunks (Eutamias): Adaptations to Aridity and High Temperature* H. CRAIG HELLER and THOMAS POULSON Department of Biology, Stanford University, Stanford, California 94305 and Department of Biology, University of Notre Dame, Notre Dame, Indiana 46556 AsstTrACT: Fecal, urinary and evaporative water losses were mea- sured at 15 C, 50-75% relative humidity for four species of western chipmunks (Eutamias) which are contiguously allopatric and _alti- tudinally zoned on the eastern slope of the Sierra Nevada, California. Evaporative loss and hyperthermia were also studied for acute exposures to 25, 35 and 40 C. Differences in total water budgets, calculated for 35 C and 11% relative humidity are not important in determining the lines of contact, starting from the alpine and descending toward the desert, between E. alpinus and E. speciosus or between E. speciosus and E. amoenus. But they may play a role in preventing EF. amoenus from colonizing the desert sagebrush habitat occupied by E. minimus. E. minimus can be active in the open areas of the hot, arid sagebrush desert by minimizing evaporative water loss and tolerating increased body heat content; this species frequently retreats to its burrows to un- load excess body heat. When large patches of shade are available from pinon pines the aggressively dominant E. amoenus can occupy the sage- brush habitat. Hence, in the field area of this study the line of contact between E. amoenus and E. minimus coincides with the lower limits of the pifion pine. INTRODUCTION Four species of western chipmunks (genus Eutamias) are zoned altitudinally on the eastern fault scarp of the Sierra Nevada, Calif. (Heller, 1971). These species do not have overlapping ranges where populations meet, but rather they maintain lines of contact and can be described as contiguously allopatric (Fig. 1). A study was undertaken to determine the relative importance of physiological adaptations and behavioral adaptations in limiting the distributions of these species (Heller, 1970). Aridity and high tem- peratures are extremely important -sources of stress in the habitats of the lower two species, E. amoenus and E. minimus. The ambient tem- peratures are never very high in the alpine habitat of E. alpinus, but levels of incident radiation are high and in late summer this habitat becomes quite arid. It was suspected that differential physiological adaptations of the species to these sources of stress might play a role in limiting their distributions. A comparative study of the water balance and tolerance to temperature stress of the four species was therefore undertaken and the results are reported herein. MATERIALS AND METHODS Animals.—Eutamias alpinus Merriam, E. speciosus frater J. A. Allen, E. amoenus monensis Grinnell and Storer and E. minimus scru- 1 Part of a dissertation submitted by H. C. Heller to the faculty of Yale University in partial fulfillment of requirements for the Ph.D. degree. 296 174 1972 HELLER AND POULSON: CHIPMUNK ADAPTATION 297 tator Hall and Hatfield (Hall and Kelson, 1959) were live-trapped on an E-W transect of the Sierra Nevada, Calif., through Yosemite National Park (38° N lat). The taxonomy and specific habitats of the chipmunks of the Sierra Nevada have been described by Johnson (1943). Laboratory conditions.—The animals were brought into the labora- tory in September 1966, 1967 and 1968, caged individually as previous- ly described (Heller and Poulson, 1970), and maintained under constant conditions of 15 + 2 C and a photoperiod of 12L:12D. Food in the form of sunflower seeds (27% protein) and Purina rat chow (23% protein, both 8 to 11% water) was available ad lib. except where indicated otherwise. Water was available ad lib. (except during water deprivation) from inverted 100-ml graduated cylinders fitted with L-shaped drinking tubes. Ad libitum water consumption. — Daily measurements of water consumption were made by recording water level in the drinking tubes every day at lights-on. Eutamias spp. show a depressed water con- sumption during their inactive season due to lower activity and lower routine metabolism (Heller and Poulson, 1970). Ad lib. con- sumptions reported are from active season records, those most eco- logically relevant to the subject of this paper. The average ad lib. water consumption for each species was determined from records of at least nine individuals for 45 to 60 days during their first full summer in captivity. The relative humidity in the laboratory during summer varied between 50 and 75% at a temperature of 15 + 0.2 C. Water deprivation—To determine the minimum water require- ments for weight maintenance and the maximum abilities of the ALPINE LONE E. ALPINUS LODGEPOLE PINE E.SPECIOSUS ZONE PINON PINE- SAGEBRUSH E.AMOENUS ZONE SAGEBRUSH W=E E. MINIMUS Fig. 1—The ‘‘Yosemite” transect of the Sierra Nevada, Calif., at 38° N lat showing the dominant vegetation of the altitudinal life zones and the alti- tudinal ranges of the four Eutamias species on the eastern slope from approxi- mately 2500 to 4000 m 175 298 THE AMERICAN MIDLAND NATURALIST 87(2) animals to minimize fecal and urinary water loss, the animals were stressed by a high protein diet and limited access to water. Four water deprivation experiments were performed: A. In early summer 1967, three EZ. alpinus, six E. speciosus and three E. amoenus were acutely stressed by progressively reducing their water rations by 25 to 50% every 2-4 days until each could just maintain body weight. B. In the early summer and also in the autumn of 1968 at least five individuals of all four species were chronically stressed by progressively reducing their daily water rations by 10% or less of their ad lib. values until the ration was reached for each on which it could just maintain body weight. C. In the summer of 1969 four individuals of each species were stressed by a diet of ground Purina rat chow mixed with 5% urea by weight. Their daily water rations were progressively reduced, as under B, until each could just maintain body weight. Water was then completely withdrawn and the urea content of the food was increased to 10% for 1 day before the urine and fecal samples were taken. Urine concentration. — Urine was collected when an animal reached the minimum daily ration of water on which it could main- tain body weight. It was deprived of all water for 1 day and was then placed in a cylindrical cage (10 x 15 cm) with a wire-mesh bottom. One hour after an animal was put into such a collection cage, a dish of mineral oil was placed underneath. Samples were collected from most urine drops under the oil with micropipettes. The melting points of the samples were measured immediately or else the micropipettes were sealed at both ends with sealing wax and frozen. Melting points were measured to + 0.01 C with a Kalber Direct Reading Biological Cryostat (Clifton Technical Physics, New York, N. Y.). Fecal water content. — Defecation was elicited by handling the animals when they were taken out of the urine collection cages after water deprivation “C.” The fresh weight of the feces +0.1 mg was determined, they were dried at 90 C , and then cooled in a desiccator until constant weight was reached. Relative medullary thickness—The relative medullary thickness of the kidneys of the animals was measured to determine their theoretical maximum potential to concentrate urine. Kidneys were preserved in 5% formalin. All excess fat was removed and the surface was quickly dried by rolling the kidney on a paper towel. The kidney was then weighed to the nearest milligram. Each kidney was cut with a razor blade along the frontal axis through the longest part of the renal papilla. The longest possible loop of Henle was measured to the near- est 0.01 mm by measuring, under a dissecting microscope with an ocular micrometer, the longest path parallel to the loops of Henle 176 1972 HELLER AND POULSON: CHIPMUNK ADAPTATION 299 extending from the cortex to the tip of the renal papilla. The relative medullary thickness (RMT) was calculated according to the formula from Sperber (1944) : Medullary Thickness x 10 ala W Kidney Size Kidney size is generally measured as length x width x thickness, but in this study the weight of the kidney was used as the index of size. For comparative purposes the RMT’s of at least four animals of each species were calculated using both weight and the product of the linear dimensions as indices of kidney size. Linear dimensions were measured with vernier dial calipers to + 0.01 mm. Evaporative water loss——Evaporative water loss was measured by direct weighing (Lasiewski et al., 1966) in a room with temperature controlled to + 0.5 C and relative humidity to + 3.0% (Environ- mental Growth Chambers, Chagrin Falls, Ohio). Throughout the experiments the water content of the air was maintained at 4.3 g/kg dry air, which is a relative humidity of 20% at 25 C, 11% at 35 CG, and 8% at 40 CG. An animal was placed in a wire-mesh cage (10 x 10 x 12 cm) suspended under a Mettler balance accurate to 0.01 g. Urine and feces were collected in a weighed pan of mineral oil under the cage. The cage was shielded from any direct air currents, and mass air flow in the room was very slow. Before and after each run at 40 C the rectal temperature of the animal was measured (+1 C) with a 36-gauge iron-constantan thermocouple. The mea- surements were made during the diurnal active period of the animals, but the lights were switched off to minimize activity. The data from a run were discarded if activity was observed during that run. Control animals handled in the same way as experimental animals, 7.e., placed in a duplicate small cage for the same period of time but kept at 16 C rather than 40 C, did not show a change in body temperature. The per cent of metabolic heat dissipated by evaporative water loss was calculated using data on the resting, postabsorptive metabolic rates of the four species (Heller and Gates, 1971). It was assumed that the metabolic consumption of 1.0 ml-Oz results in the production of 4.8 cal and that the heat of evaporation of 1.0 ml H.O at slightly less than core body temperature is 580 cal. RESULTS Ad lib. water consumption.—The daily ad lib. water consumption of E. alpinus, E. speciosus and E. amoenus in the laboratory during their active season averages 16% of body weight; the average value for E. minimus is 11% of body weight (‘Table “1). The ad lib. water consumption of E. minimus is significantly lower than that of E. amoenus (p < .05) and E. speciosus (p <.05) but not that of E. alpinus (p < .10, t-test). Minimum water requirement for weight maintenance.—The weight 177 300 THE AMERICAN MipLANpD NATURALIST 87(2) specific minimum daily consumption (Table 1) of E. amoenus was significantly lower than that of E. speciosus (p < .05) and tended to be lower than that of E. alpinus (p < .10). This indicates that E. amoenus has a higher capacity for water conservation under water deprivation stress than do the other two species. E. minimus does not show a minimum consumption significantly different from any of the other three species. The average extent to which each species can decrease its water TasLe 1.—Mean water consumption, fecal water content, RMT, and urine concentration Eutamuias Parameter alpinus speciosus Body weight $97 L=0n4 LO eZ: (e)=E1 S.E. n=16 n=22 Ad lib. water consumption 16. l==2..°6 fon GEEOs 29 (per cent Wt,) +1 S.E. n= 9 n=11 Minimum water consumption Ue Dae 7 7s 9220) 7 (per cent Wt,) +1 S.E. n= 8 n=12 Fecal water content AO, 922253 ae Wa=ie © (per cent wet wt.) +1 S.E. n= 5 n= 7 Relative medullary thickness 1 == Oat 9.32£0.14 a=) S.i0- n= 5 n=14 Urine concentration (Melting-pt. depression, C) : ue Mean maximum 7.20 Gn n=10 n=13 Five maximum values > 9.53 8.87 Heth: 8.32 7.50 7.85 7.50 7.50 7.16 Dold TaBLeE 1.—(continued) Eutamias Parameter amoenus minimus Body weight 42. 4+0. 9 gon 2-203 (a) 210 S:E n=18 n=18 Ad lib. water consumption Ga Ons On S-=05n8 (per cent Wt,) £1 S.E. n=11 n= 9 Minimum water consumption 5. 60. 4 65 322056 (per cent Wt,) £1 S.E. n= 9 n= 6 Fecal water content 47. 2=1. 0 AGa le=22..0 (per cent wet wt.) +1 S.E. n= 6 n= 3 Relative medullary thickness 10.39=0.16 12.08£0.35 Sal ork. n= n=15 Urine concentration (Melting-pt. depression, C) itt — Mean maximum 7.93 8.02 n= 9 n= 9 Five maximum values >9.53 >9.53 S995 >9.53 >9.53 > 9.53 >9.53 8.45 7.17 8.27 178 1972 HELLER AND POULSON: CHIPMUNK ADAPTATION 301 requirement when stressed 1s 65% for E. amoenus, 55% for E. alpinus, 50% for E. speciosus and 43% for E. minimus. ‘The already low ad lib, consumption of E. minimus may allow it less scope for additional water conservation than is available to EL. amoenus. Fecal water content——No differences were evident in the fecal water content of the four species after water deprivation and urea loading. The means were between 46 and 50% of wet fecal weight (Table 1). Maximum urine concentration.—All four species produced very concentrated urines when deprived of water or deprived of water and urea-loaded (Table 1). E. minimus and EF. amoenus produced the most and E. speciosus the least concentrated urines, but there is a great deal of overlap in the maximal concentrations of the urine pro- duced by the four species. All freshly dropped urine samples contained numerous unidentified small crystals. If urine concentration is at all important regarding competition, then the maximum urine concentration that individuals of each species can achieve will determine whether any species can occupy an arid habitat that is physiologically inaccessible to other species. Melting- point depressions showed a great deal of variability; for example, one animal during a single 12-hr collecting period can drop samples dif- fering in their melting points by 3-4 C. “Fright diuresis” resulting from placing the animal in the urine collection cage may have con- tributed to this variation in spite of the precautionary measure of not collecting urine samples during the Ist hr an animal was in the cage. Also, there may be species differences in fright diuresis, and, there- fore, maximum values were taken from the data. The mean maximum melting points (Table 1) were determined from the maximal value for each individual even though that individual may have been used in more than one experiment. The five maximum values given are the five highest values for each species. The ranges and means for E. minimus and E. amoenus are in reality lower, but the cryostat used did not measure below —9.53 C. Relative medullary thickness—RMT?’s calculated from the weight of the kidney agree well with RMT’s calculated from the linear mea- surements, but in the range of measurements for the Eutamias species RMT by weight averages 1 RMT unit higher than RMT by linear dimensions. The RMT’s of all four species are significantly different from each other (Table 1), with that of FE. minimus > E. alpinus > LE. amoenus > E. spectosus. Evaporative water loss—There are no significant differences be- tween the weight specific rates of evaporative water loss of E. alpinus, E. speciosus and E. amoenus at 25 C, but E. minimus shows a signifi- cantly higher value than any of the other three species (Table 2). The values for evaporative water loss/metabolic heat production at 25 C are in Table 2. Evaporative water loss accounts for 21-32% of metabolic heat production in all four species at this temperature. 179 302 THE AMERICAN MipLaNp NATURALIST 87(2) The rate of evaporative water loss of E. amoenus at 35 C showed great variability and overlapped that of all the other species. The value for E. minimus at 35 C is significantly lower than that for E. alpinus and E. speciosus. This relative shift in the ranges of values for the four species results from roughly parallel, significant increases in the evaporative water losses of EF. alpinus, E. speciosus and E. amoenus between 25 and 35 C, whereas the evaporative water loss rate of E. minimus remained the same at 35 as it was at 25 C. The evaporative water loss rates of EF. alpinus, E. speciosus and E. amoenus increased between 25 C and 35 C while their metabolic rates decreased slightly; hence, the proportion of heat production dissipated by water loss (E.W.L./M.H.P.) increased. The E.W.L./M.H.P. ratio of E. mini- mus remained constant, however, over this same temperature range. The maintenance of a low E.W.L./M.H.P. ratio conserves water and is adaptive in the arid habitat of E. minimus. The rates of evaporative water loss of all four species increased three- to fourfold between 35 C and 40 C (Table 2). EF. minimus still had the lowest mean value, significantly lower than EF. alpinus and E. amoenus (p < .05, t-test). TasLe 2.—Mean evaporative water and heat loss rates, metabolic rates and heat storage rates Parameters and Eutamias conditions alpinus speciosus Evaporative water loss rate (mill x 103/e¢/hr) ==1 S:E: Pe 23-6 Sd == O52 2eo == OES n= 4 n= 4 T, =35C 6. 22 0:4 Sy ibe == 105 n= 4 n= 4 T, =40C DA Ose 1S / MESO) ee lets} n=17 n=22 Evaporative heat loss rate at 40 C (cal/45 min) +1 S.E. Silse Oasis 2) p20 ea ola Metabolic rates (Heller and Gates, 1971) (ml\0,-e“4hr-*): = 1 SE. T, =29¢G N65 -03 Ieee 03 n= 4 n= T, =35C 1.434 .04 47.01 n= 3 n= E.W.L. x 100/M.H.P. (per cent) Br en ©; 23:9 30.4 T, = 35C 50.7 41.1 Rate of rise in body-heat content at T, = 40 C (cal/¢/45 min) =1 S.E. 2.29 0.68 2,20 == 0:65 Mean body size (g) +1 S.E. SOL les0s 9 HO, gas aes n=16 n=22 (otal cal/45 min) 2=1) Sik: OB ee 293m 15 6e Oo, 180 HELLER AND PoULSON: CHIPMUNK ADAPTATION 303 1972 All of the animals showed hyperthermia at 40 C. Therefore, uni- form 45-min exposures were used to measure evaporative water loss at this temperature. Body-temperature changes were recorded to allow calculation of the rates of heat storage. The results are pre- sented in Table 2 and Figure 2 on a weight specific basis and in Figure 3 on an absolute basis. The specific heat of animal tissue was taken as 0.8 cal/g. The areas shown in Figures 2 and 3 for each species enclose all of the data points obtained for that species. There are no significant differences in rate of weight specific in- crease in body heat content at 40 C. Significant differences in calories lost by evaporation exist, however, between E. minimus and E. alpinus, E. minimus and E. amoenus, and E. alpinus and E. speciosus. E. speciosus is significantly higher in both parameters than the other three species when the data are plotted as total calories lost through evaporative water loss vs. total calories gained through hyperthermia for a 45-min exposure (Fig. 3). The other three species are signifi- cantly different from each other in total calories lost through evapora- tive water loss but not in total calories gained through hyperthermia. TABLE 2.—(continued ) Parameters and Eutamias conditions amoenus minimus Evaporative water loss rate (ml x 108/e/7hr) 1S. Tm 29.C 3. 4+ 0.4 49 = 0.2 n= 3 n= 4 T, = 39 C 6. O22 057 4:5. == 10:2 n= 4 n= 8 T, =40C 20. 7 1.4 1466 == 025 n=18 n=18 Evaporative heat loss rate at 40 C (cal/45 min) =1 S.E. B23 8ea lian 0 21/7. 8= 17. 0 Metabolic rates (Heller and Gates, 1971)(ml0, ghr-?) £1 S.E. T, =25C 1:82 .06 [eGt==s 202 n= n= 4 dear he © 7 O0== 7209 1. 61==5 415 n= 3 n= 5 E.W.L. x 100/M.H.P. (per cent) Te 2oG PALS ODA) T, = 35C 41.2 33:8 Rate of rise in body-heat content at T, = 40C (cal/g/45 min) +1 S.E. 201E=50:31 2.92+ 0.49 Mean body size (¢g) +1 S.E. 42. 4+ 1. 8 Sone a aan n=18 n=18 (Total cal/45 min) +1 S.E. 84. 5+ 4. 9 101..9= 5.4 181 304 THE AMERICAN MIpLAND NATURALIST 87(2) TotraL WATER BUDGETS Any adaptations to a hot, arid habitat that are due to interspecific differences in water balance can best be judged and compared by constructing total water budgets for a given set of conditions (Table 3). The conditions used in the present study are relatively hot and arid, but not extreme: 35 C ambient temperature, 11% relative humidity, and a diet of air-dried sunflower seeds. All calculations were made for 4-hr periods because the aboveground activity of FE. minimus in nature is mostly limited to a 4-hr period before noon (Heller, 1970). The expected total water requirement is calculated by summing fecal, urinary and evaporative water loss. The water from food, pre- formed water and water derived from oxidative metabolism is sub- —_ w _ i) — _ = o wo at Mean Sum G'-45MIN' LOST BY EVAP. H20 LOSS of Coordinates 3F Alpinus 12.4+0.8 CAL: Speciosus 9.8+0.9 Amoenus 9.6+0.7 1 Minimus 9.140.9 2 3 4 CAL: G45 MIN’ GAINED BY RISE IN Tp Fig. 2.—Calories per gram gained through hyperthermia and calories per gram lost through evaporation when resting animals are exposed to 40 C, 8% R.H. for 45 min. The areas enclose all of the data points for each species. S = E. speciosus, Al = E. alpinus, M = E. minimus, and the remaining area is for E. amoenus. The sum of the coordinates of each data point is an index of the degree to which the conditions stressed the animals (see Discussion). The mean sum of the coordinates for each species is given at the lower left. Data in Table 2 182 1972 HELLER AND POULSON: CHIPMUNK ADAPTATION 305 tracted from the total water requirement to get the free water requirement. The weight specific free water requirement is multiplied by the species’ mean body weight to arrive at the absolute amount of free water an animal of that species must have to remain in neutral energy balance under the hypothetical conditions for 4 hr without suffering a net water loss. These calculations make no allowance for activity, nor are the conditions unusually stringent in comparison to the natural habitat. A T, of 35 C, which is below the upper critical temperature of all four species, is realistic for the habitat of E. mini- mus near noon on a clear summer day, but the soil surface tempera- tures and temperatures of the air strata that this species is exposed to are considerably higher. Fecal water loss—The dry weight of feces produced per gram of animal (unpublished data) during measurements of routine metab- olism at 5.0 C (Heller and Poulson, 1970) was corrected for the lower metabolic rates at 35 C (Heller and Gates, 1971). The fecal water loss per gram of animal per 4 hr was calculated using the data on fecal water content after water deprivation (Table 1). Urinary water loss—The expected urinary water loss was calcu- lated using data on metabolic rate, protein content and caloric value of food, and urine concentration. Sunflower seeds have a caloric =e LOST THROUGH EVAP. WATER LOSS xX 10 CALORIES Temp.=40°C Time =45 min 50 100 150 200 250 CALORIES GAINED THROUGH RISE IN Tp Fig. 3.—Total calories gained through hyperthermia and total calories lost through evaporation when resting animals are exposed to 40 C, 8% R.H. for 45 min. Notation is the same as in Figure 2. Data in Table 2 183 306 THE AMERICAN MiIpLaNp NATURALIST 87 (2) value of 6.1 kcal/g and a protein content of 28%. Assuming the standard N content of protein, 16%, 7.52 x 10° N must be ex- creted for every kcal produced from the metabolism of sunflower seeds. Grarns of N/kcal were multiplied by the metabolic rate of the animal in kcal/g animal/4 hr to arrive at g N excreted/g animal/4 hr. Assuming all N is excreted as urea and each mole of urea contains two moles of N, dividing g N/g animal/4 hr by 0.028 gives mM urea/g animal/4 hr; and dividing that figure by the maximal urine concentration in mM urea/ml gives the minimal weight specific urine volume or urinary water loss for a 4-hr period. The maximum urine concentration was inferred from the RMT’s. Electrolytes from the food also contribute to the total osmolarity of the urine. We have not taken this into account, so our calculated urinary water loss will be slightly too low. Evaporative water loss—Evaporative water loss in ml/hr/g animal was taken from Table 2 and multiplied by four. Water gain—The water the organism acquires from ingested food depends on the preformed water content of the total food ingested and the water formed from the oxidation of the ingested food which is assimilated. The amount of seeds assimilated was calculated from the metabolic rate at 35 C and the caloric value of sunflower seeds. The water derived from the sunflower seeds assimilated was calculated by dividing grams of seeds into grams of protein, grams of fat and grams of carbohydrate, and each was multiplied by the water of oxidation it yields per gram. The average composition of sunflower seeds (Winton and Winton, 1932) is 8% water, 28% protein, 46% fat and 12% carbohydrate. Metabolized protein yields 0.40 g H,O/g; fat yields 1.07 g¢ H.O/g, and carbohydrate yields 0.56 g H,O/g >) (Schmidt-Nielsen and Schmidt-Nielsen, 1951). TasLe 3.—Expected water budgets of resting animals exposed to 35 C, 11% R.H. for 4 hr in nature Eutamias alpinus speciosus amoenus minimus Water loss (ml g-1 hr! x 4) Fecal water loss .0004 .0005 .0006 .0004 Urinary water loss .0013 .0016 .0017 .0014 Evaporative water loss .0248 .0204 .0232 0.180 Total water loss .0265 .0225 .0255 .0198 Water gain (ml g-? hr! x 4) Water of oxidation .0031 .0031 .0036 .0034 Preformed water .0005 .0006 -0006 .0006 Total water gain .0036 .0037 .0042 .0040 Free water requirement (= total loss — total gain) (ml g-! hr-1 x 4) 0229 .0188 O23 .0158 Free water requirement per animal (ml hr x 4) .894 33) .895 554 184 1972 HELLER AND POULSON: CHIPMUNK ADAPTATION 307 The preformed water in all of the food ingested contributes to the water budget even if all of that food is not assimilated. So the total amount of sunflower seeds ingested times their water content gives the amount of preformed water in the food. The total amount of sunflower seeds ingested can be determined from the amount assimi- lated if the efficiency of assimilation is known. The efficiency of assimilation was calculated by comparing the caloric value of sun- flower seeds ingested at 5 C (Heller and Poulson, 1970) with meta- bolic rate at 5 C as measured by O2 consumption (Heller and Gates, 1971). The values for all species were between 64 and 68%. It was assumed that the efficiency of assimilation would be the same at 35 C. Two studies on steers and one on rabbits at unspecified temperatures show calculated assimilation efficiencies of 68, 69 and 66%, respective- ly (Brody, 1945, p. 80). The assimilation efficiencies of English sparrows varied only 9% between 0 and 34 C (Davis, 1955). The maximum was at 18 C, and the assimilation efficiency at 4 C was 77% and at 34 C, 78% for birds on a 10-hr photoperiod. Free water requirement.—The amount of free water required per gram animal per 4 hr is obtained by subtracting total water acquired through food from total water loss. This figure for each species is then multiplied by the mean weight of that species to arrive at total re- quirement of free water per animal per 4 hr. Calculated water budgets—Over 90% of the water loss of all species 1s attributable to evaporation at 35 C and 11% relative humidity (Table 3). E. minimus has the lowest weight specific water require- ment due to its low evaporative loss, and its total water requirement 1s considerably less than that of the other three species. The total water requirement of EF. speciosus 1s considerably greater than that of the other three species. DiIscussION Differences exist in the water balance of the four species of Eu- tamias studied, but are any of these differences of sufficient magnitude to physiologically exclude any of the species from the habitat of any other? It has been shown that E. speciosus 1s excluded from the more arid habitats of FE. alpinus and E. amoenus by the aggressive dom- inance of those two species (Heller, 1971), so physiological limita- tions on E. speciosus are probably not primary in restricting its local distribution. The interesting case is that of E. minimus and E. amoenus, both of which are found in hot, arid habitats. EF. amoenus ageressively excludes E. minimus from E. amoenus habitat (Heller, 1971), but is EZ. amoenus physiologically excluded from FE. minimus habitat? To answer this question with respect to water balance it is necessary to compare the species’ adaptations to all sources of water loss and to calculate their total water budgets. Total water loss is the sum of fecal, urinary and evaporative water losses. No differences were found in fecal water loss, so only urinary and evaporative water losses will be discussed in detail. Urinary water loss——Relative Medullary Thickness is an index 185 308 THE AMERICAN MIDLAND NATURALIST 87(2) directly related to aridity of habitat (Sperber, 1943) and the maxi- mum possible urine-concentrating ability (B. Schmidt-Nielsen and R. O'Dell, 1961; Heisinger and Breitenbach, 1969), but it is also related to body size (Blake, 1967). If one determines the differences in the RMT’s of the Eutamias spp. expected solely on the basis of body size, then the residual differences can be implicated as adaptation to aridi- ty. RMT is plotted as a function of body size in Figure 4B. The lower line was fitted by eye to the mean RMT’s of samples of E. minimus, E. amoenus, E. quadrivittatus, E. umbrinus, E. townsend, Tamias striatus and Spermophilus lateralis (Blake, 1967). Blake’s RMT’s are consistently lower than ours. One RMT unit of this difference 1s attributable to our use of kidney weight as the index of kidney size, and at least 0.6 RMT units difference are due to Blake’s selection of data for lowest RMT’s. The balance of the discrepancy is unexplained. A line drawn parallel to Blake’s line and passing through the RMT values for E. speciosus also passes through the mean value for FE. amoenus, but the values for E. minimus and E. alpinus are consider- ably above this line. This indicates that the RMT differences between A FR. PT. °C 30 40 60 90 R. M. T. BODY WT. (G) Fig. 4A.—Maximum urine concentration (freezing point depression) plotted vs. mean R.M.T. @& = E. alpinus, A, = E. speciosus, Q = E. amoe- nus, [ ] = E. minimus. Solid dots are from B. Schmidt-Nielsen and O'Dell (1961) and left to right represent beaver, pig, man, dog, cat, rat, kangaroo rat, jerboa and sand rat. 4B.— Relative Medullary Thickness vs. body weight. The lower line (Blake, 1967) represents five Eutamias species, Tamias striatus and Spermophilus lateralis, all from relatively mesic habitats. The dot (Blake, 1967) represents a population of E. minimus from an arid environment. The upper line was drawn parallel to the lower line and made to pass through the mean value for E. speciosus (this study). Vertical lines are ranges, horizontal lines are means, and bars represent two standard errors on each side of the mean. Data in Table 1 186 1972 HELLER AND POULSON: CHIPMUNK ADAPTATION 309 E. speciosus and E. amoenus could be expected solely as adaptations related to differences in body size, but that EL. minimus and E. alpinus show a relatively greater adaptation to aridity in their kidney mor- phologies. The high maximal urine concentrations of all four Eutamias species are in the range of other small desert rodents (Schmidt- Nielsen et al., 1948; Schmidt-Nielsen and O’Dell, 1961; Hudson, 1962; Hudson and Rummel, 1966; Carpenter, 1966; MacMillen and Lee, 1969). An accurate comparison of RMT and maximal urine concentration in chipmunks is not possible because the maximal melting-point depressions of E. minimus and E. amoenus samples were beyond the range of the cryostat. The maximum values found in this study plotted as a function of RMT correlate well with data for other animals (Fig. 4A). The values from this study would fall even closer to Schmidt-Nielsen and O’Dell’s curve if the actual maximum urine concentrations for E. minimus and E. amoenus were known and if the correction of —1 RMT unit were made so that our values were equivalent to those based on linear measurements of the kidney. Evaporative water loss.—Evaporative water loss is an effective heat-dissipating mechanism in a hot, arid environment (Hudson, 1962, 1964), but also the main source of water loss for a small animal (Schmidt-Nielsen and Schmidt-Nielsen, 1951). If an animal adapts to the aridity of the environment by reducing evaporative water loss, concomitantly it must increase its efficiency of dealing with heat stress via alternative mechanisms. E. alpinus, E. speciosus and E. amoenus dissipated a greater per cent of metabolic heat through the evaporation of water at 35 C than they did at 25 GC, but E. minimus maintained a constant E.W.L./M.H.P. ratio over this temperature range (Table 2). Therefore, E. minimus must be able to increase the efficiency of its evaporative cooling (e.g., by decreasing cutaneous relative to pulmonary loss), or to enhance the effectiveness of con- vection, conduction or radiation as T, approaches Ts, or to permit a slight increase in body-heat content. Ty was not measured during the 35 C evaporative-water-loss experiments; however, the possibility that E. minimus used heat storage to maintain a low E.W.L./M.H.P. ratio at 35 C is given credence by the fact that at 40 C E. minimus showed hyperthermia more than the other three species. An increase in Tp of E. minimus of only 0.12 G/hr would be equivalent in calories to the increase in evaporative water loss shown by the other species between 25 and 35 C. At a T, of 40 C heat must be lost through the evaporation of water, or alternatively, the heat content of the body must increase if the T, starts out below 40 C. The data in Figure 2 indicate that the strategy of E. minimus to cope with dry heat is to depend more on hyperther- mia and less on evaporative water loss during short exposures than do the other three species. The sum of increase in heat content through hyperthermia and heat loss by evaporation (Fig. 2, insert) is an indi- cation of the degree to which the animals were stressed by dry heat. 187 310 THE AMERICAN MIDLAND NATURALIST 87 (2) Although £. minimus was stressed the least, the differences between it and EF. speciosus and E. amoenus are not significant (p > .05, t- test). E. alpinus was stressed by the dry heat significantly more than the other species. The low E.W.L./M.H.P. ratio of E. minimus (Table 2) and its tendency to show hyperthermia in dry heat (Fig. 2) indicate that in nature it may rely chiefly on hyperthermia to cope with its hot, arid environment. Like the antelope ground squirrel which is found in the same type of habitat (Hudson, 1962), &. minimus probably alter- nates periods of aboveground activity, during which it allows its body- heat content to increase, with periods of rest in a burrow where it can dissipate the incurred heat load. E. minimus was observed to spend less and less time aboveground as the T, rose and reached its maxi- mum in early afternoon (Heller, 1970). Body size.—Body size is also an adaptive feature in a hot, arid environment. Regardless of the weight specific values, it is the total amount of water evaporated which must be replenished and the total increase in heat content which will have to be dissipated. It is inter- esting to note the relative positions of the data “areas” in Figure 3 where total calories gained through hyperthermia and total calories lost through evaporation are plotted. E. speciosus experiences the greatest total flux of energy and EF. minimus the least. There is almost complete separation of E. minimus and E. amoenus, both of which are of similar body sizes and are from hot, arid habitats. Water budgets—The calculation of the total water budgets for the four species (Table 3) reveals that evaporation accounts for over 90% of the total water loss under the experimental conditions. This high evaporative water loss relative to urinary loss probably holds in nature even though the evaporative water loss was not measured on animals acclimated to high T,. The antelope ground squirrel, which weighs about 90 g, does not show significant differences in evaporative water loss between individuals that are and are not acclimated to 35 C (Hudson, 1962). The evaporative loss of this species at 35 C is similar to the values for the Eutamias species reported here. Water budgets calculated for aboveground summer environmental conditions indicate that significant improvements in the water con- serving ability of small diurnal mammals can only occur through the reduction of evaporative water loss. Even relatively large changes in the abilities of the closely related Eutamias species to decrease fecal and urinary water loss would have a rather small effect on the total water loss incurred while active aboveground. When the animals are in the atmosphere of a burrow, the urinary and fecal water losses would be a larger per cent of the total loss, and, therefore, a larger per cent of the 24-hr water budget than of the 4-hr budget for above- ground. To be sure, there have been strong selective pressures to achieve the high renal efficiency observed in these animals, but these renal adaptations to aridity are not of primary importance in physio- 188 1972 HELLER AND PouLSON: CHIPMUNK ADAPTATION 3it logically limiting the time intervals over which these diurnal animals can be active aboveground in the desert environment. Does the fundamental niche of E. amoenus include the habitat of E. minimus in the study area?—E. minimus is excluded from the habitat of E. amoenus by the aggressive dominance of FE. amoenus; therefore, E. minimus has a realized niche smaller than its fundamental niche in the study area (Heller, 1970, 1971). What prevents E. amoenus or any of the other species from colonizing the habitat of E. minimus? The habitat of E. amoenus is also hot and arid, but it contains numerous pifion pine trees. The pinion pines provide large patches of shade in comparison to the small dispersed patches of shade available in the sagebrush habitat of FE. minimus. Both E. amoenus and E. minimus experience similar T,’s and relative humidities, but the large patches of shade enable E. amoenus to escape from direct incident radiation and to avoid high soil-surface temperatures. EF. amoenus frequently climbs in the pinon pines and sits on well- shaded branches where heat loss by convection and radiation is maximized. On the edge of Diamond Valley near Woodfords, Calif., the range of FE. amoenus extends far beyond the limit of pinon pines and into the sagebrush-shrub habitat (personal observation). The desert shrubs in that area, however, are more dense and generally twice as tall as they are on the Yosemite transect; hence, large patches of shade were available at all hours of the day. No E. minimus were trapped in this habitat. In spite of similar body sizes, E. minimus is better adapted to coping with dry heat than is E. amoenus and may use a different strategy for doing so. The activity pattern of E. minimus in nature indicates that after 11 am, P.D.S.T., this species, in contrast to the others, spends most of its time in its burrow (Heller, 1970). Energy budget calculations (Heller and Gates, 1971) indicate that E. minimus is physiologically prevented from remaining active above- ground for the greater portion of the day in spite of its adaptation to dry, hot sagebrush desert. If E. minimus is marginally adapted to the sagebrush desert habitat in the study area, then it is certain that F. amoenus and the other two species are physiologically incapable of colonizing this habitat. Hence, the realized niche of E. minimus in the study area is outside of the fundamental niches of the other species. This and other studies (Heller and Gates, 1971) have shown con- siderable overlap in the physiological adaptations of the four species of chipmunks with the most marked differences between Eutamias minimus and the other three species. The most important present-day factor that determines their altitudinal zonation is interspecific aggres- sion with some reinforcement by habitat selection both by the aggres- sive and subordinate species (Heller, 1971). Thus E. alpinus is aggressively dominant to FE. speciosus and E. amoenus is dominant to both E. speciosus and E. minimus. The only case where physiology helps to explain the contiguously allopatric zonation is with the £. amoenus/E, minimus contact. Our conclusion from the present report 189 12 THE AMERICAN MiIpLanp NATURALIST 87 (2) is that the fundamental niche of E. amoenus does not include the hot, arid sagebrush habitat occupied by E. minimus. Thus, E. amoenus is the only one of the four species which is physiologically excluded from another species habitat. Acknowledgments.—This research was supported by NSF Grant GB-6212 to T. L. Poulson, an N.D.E.A. Title IV Fellowship to H. C. Heller, and funds from the Department of Biology, Yale University. We are grateful to Yosemite National Park for permission to do field work and to Mr. and Mrs. Gary Colliver for untiring assistance with field work. Also we are greatly indebted to Mr. Vincent Salerno for assistance in the laboratory. REFERENCES Buaxe, B. H. 1967. A comparative study of energy and water conservation throughout the annual cycle in ground-dwelling Sciuridae. Ph.D. Dis- sertation, Yale University. 188 p. University Microfilms, Ann Arbor, Michigan. Bropy, S. 1945. Bioenergetics and growth, with special reference to the effi- ciency complex in domestic animals. Reinhold Publishing Co., New York. 1023 p. CarpENTER, R. E. 1966. A comparison of the thermoregulation and water metabolism in the kangaroo rats Dipodomys agilis and Dipodomys mer- riami. Univ. Calif. Publ. Zool., 78:1-36. Davis, E. A. 1955. Seasonal changes in the energy balance of the English sparrow. Auk, 72:385-416. Hatt, E. R. anp K. R. Ketson. 1959. The mammals of North America. Vol. I. The Ronald Press Co., New York. 546 p. Hersincer, J. F. anp R. P. BrerrenspacH. 1969. Renal structural characteris- tics as indexes of renal adaptation for water conservation in the genus Sylvilagus. Physiol. Zool., 42:160-172. Hetter, H. GC. 1970. Altitudinal zonation of chipmunks (genus Eutamias) : Interspecific aggression, water balance, and energy budgets. Ph.D. Dis- sertation, Yale University. University Microfilms, Ann Arbor, Mich. . 1971. Altitudinal zonation of chipmunks (genus Eutamias): Inter- specific aggression. Ecology, 52:312-319. AND D. M. Gates. 1971. Altitudinal zonation of chipmunks (genus Eutamias): Energy budgets. Ibid., 52:424-433. AND T. L. Poutson. 1970. Circannian rhythms: II. Endogenous and exogenous factors controlling reproduction and hibernation in chipmunks (Eutamias) and ground squirrels (Spermophilus). Comp. Biochem. Physiol., 33:357-383. Hupson, J. W. 1962. The role of water in the biology of the antelope ground squirrel Citellus leucurus. Univ. Calif, Publ. Zool., 64: 1-56. . 1964. Temperature regulation in the round-tailed ground squirrel Citellus tereticaudus. Ann. Acad. Sci. Fenn. Ser. A, IV, Biol., 71: 217-233. AND J. A. RumMeEL. 1966. Water metabolism and temperature regula- tion of the primitive Heteromyids Liomys salvani and Liomys irroratus. Ecology, 47:345-354. Jounson, D. H. 1943. Systematic review of the chipmunks (genus Eutamias) of California. Univ. Calif. Publ. Zool., 48:63-148. 190 1972 HELLER AND PoULSON: CHIPMUNK ADAPTATION 513 LasiEwskl, R. G., A. L. Acosta AND M. H. Bernstein. 1966. Evaporative water loss in birds — II. A modified method for determination by direct weighing. Comp. Biochem. Physiol., 19:459-470. MacMitten, R. E. anp A. K. Lee. 1969. Water metabolism of Australian hopping mice. Ibid., 28:493-514. ScumipT-NIELsEN, B. anp K. Scumipt-NIELsSEN. 1950. Evaporative water loss in desert rodents in their natural habitat. Ecology, 31:75-85. AND 1951. A complete account of the water metabolism in kangaroo rats and an experimental verification. J. Cell. Comp. Physiol., 38:165-181. AND R. O’De Lt. 1961. Structure and concentrating mechanism in the mammalian kidney. Amer. J. Physiol., 200: 1119-1124. , K. Scumipt-NiELsen, A. Brokaw anp H. SCHNEIDERMAN. 1948. Water conservation in desert rodents. J. Cell. Comp. Physiol., 32: 331-360. SperBer, A. 1944. Studies on the mammalian kidney. Zool. Bidrag Uppsala, 22: 249-432. Winton, A. L. anp K. B. Winton. 1932. The structure and composition of foods. Vol. I. John Wiley and Sons, Inc., New York. 613 p. SusMItTTep 5 Marcu 1971 AccEepTepD 15 Aprit 1971 191 THE OXYGEN CONSUMPTION AND BIOENER- GETICS OF HARVEST MICE OLIVER P. PEARSON Museum of Vertebrate Zodlogy, University of California, Berkeley ATES of metabolism or of oxygen R consumption have been reported for many species of small mam- mals, but little effort has been made to relate such measurements to the energy economy of small mammals in the wild. Such effort has been avoided because the rate of metabolism varies so much with changes of the ambient temperature and with activity of the animal. I believe, however, that these variables can be handled with sufficient accuracy so that one can make meaningful estimates of the 24-hour metabolic budget of free-liv- ing mice in the wild. In this study I have measured the oxygen consumption of captive harvest mice under different con- ditions, and from these measurements I have estimated the daily metabolic ex- change of wild harvest mice living in Orinda, Contra Costa County, Califor- nia. The harvest mice used in the study (Reithrodontomys megalotis) are noctur- nal, seed-eating rodents living in grassy, weedy, and brushy places in the western half of the United States and in Mexico. In Orinda they encounter cool wet win- ters (nighttime temperatures frequently slightly below 0° C.) and warm dry sum- mers (daytime temperatures sometimes above 35° C., but nights always cool). They do nothibernate. MATERIAL AND METHODS Five adult harvest mice were caught on January 29 and 30, 1959, and were kept in two cages in an unheated room with open windows so that the air tem- perature would remain close to that out- side the building. They were fed a mix- ture of seeds known as “‘wild bird seed.”’ Metabolic rates were tested between Jan- uary 29 and April 1 in a closed-circuit oxygen consumption apparatus similar to the one described by Morrison (1947) but without the automatic recording and re- filling features. All tests except the 24- hour runs were made during the daytime and without food. Since harvest mice are strongly nocturnal, several hours had usually elapsed between their last meal and the measuring of their oxygen con- sumption. When placed in the apparatus, the mice usually explored the metabolic chamber and groomed their fur for about half an hour and then went to sleep on the wire mesh fioor of the chamber. One hour or more was allowed for the animals to become quiet and for the system to come to temperature equilibrium. The animals usually were left in the chamber until from five to ten determinations of oxygen consumption had been made, during which they had remained asleep or at least had made no gross movements. Each determination lasted between 9 and 24 minutes. The mice were weighed when they were removed from the apparatus. Oxygen consumptions are reported as volume of dry gas at 0° C. per gram of mouse. RESULTS SIZE X RATE OF METABOLISM Adult harvest mice weigh between 7 and 14 grams. Larger individuals con- sume oxygen at a lower rate per gram of 192 METABOLISM OF body weight (lig. 1). lor example, at 12°C. a 12-gram mouse would use only 1.17 times as much oxygen per hour as an 8-gram mouse, although it is 1.5 times as heavy. The various points in the regres- sion of body weight against rate of oxy- gen consumption can be fitted ade- quately with a straight line, and from the slopes of such lines illustrating the re- gression at different ambient tempera- tures it may be seen (Fig. 1) that at cold temperatures a variation of 1 gram in body weight causes a greater change in metabolic rate than at 30°C. At 1°, 12°, and 24° a change of 1 gram in weight is associated with a change in oxygen con- sumption of 0.98, 0.48, and 0.35 cc/g/hr, respectively. At warm and moderate temperatures there was little variation in the measure- ments of each mouse during any one run (Fig. 1), but at 1° C. the variation was sometimes enormous. Since each meas- urement was made over a period while the mouse was inactive, the variation must stem from a real difference in the resting metabolism of each mouse at different times. I beheve that lability of body tem- perature is the cause. Harvest mice ex- posed to cold and hunger in box traps sometimes are tound to be torpid and with a cold body temperature. If they are tagged and released, they can be re- captured in good health at subsequent trappings, demonstrating that harvest mice have a labile body temperature and can recover irom profound hypothermia. During the metabolic tests at 1° C., espe- cially those with the mouse in a nest, there was a tendency for most of the measurements to lie at one level; but there would be a few very low readings and a few intermediate readings, pre- sumably as the animal entered and emerged from the low-metabolic condi- tion (best shown by the 114-gram mouse in Tig. 1). In response to cold coupled 193 HARVEST MICE 153 with restful surroundings, as in a nest, the animals probably relaxed their tem- perature control temporarily. This ex- planation seems plausible in view of the known lability of the body temperature of some rodents such as Peromyscus (Morrison and Ryser, 1959), Dipodomys (Dawson, 1955), and Perognathus (Bar- tholomew and Cade, 1957) under similar circumstances. Birds permit their body temperature to drop about 2° C. when they sleep at night, and this is accom- panied by a drop of as much as 27 per cent in rate of metabolism (De Bont, 1945). The 40 per cent drop shown by some of the mice may have been accom- panied by a drop in body temperature of several degrees. RESTING METABOLISM AT DIFFERENT TEMPERATURES Since the weights of adult harvest mice vary so much, it is desirable to eliminate the size variable by adjusting all rates of metabolism to a single average size (9 grams). This has been done by using the serles of regression lines in Figure 1. Where each of these lines crosses the 9- gram ordinate, that value is taken as the appropriate rate for a “standard” 9-gram harvest mouse and is used in Figure 2. The middle curve in Figure 2 shows that the minimum rate of oxygen con- sumption of harvest mice (2.5 cc/g/hr for a 9-gram mouse) is reached at the relatively high ambient temperature of 33° or 34° C. and that there is almost no zone of thermal neutrality. Rate of me- tabolism almost certainly begins to in- crease before 36° C. is reached so that the zone of minimum metabolism could not include more than 3°. The critical tem- perature (33-34°) is remarkably close to the upper lethal temperature. The single animal tested at 37° died after two hours at this temperature but provided several good measurements before entering the OXYGEN CONSUMPTION (CC/G/HR) , Ke) II \2 13 WEIGHT IN GRAMS OXYGEN CONSUMPTION (CC/G/HR) 8 9 10 I l2 I3 WEIGHT IN GRAMS Fic. 1.—The relation between body weight and rate of oxygen consumption under difierent conditions, showing also the variation in individual measurements. Mach cluster or vertical array of points represents a series of values obtained from a single individual. 194 METABOLISM OF HARVEST MICE final coma. Because of the large exposed surface of calcium chloride and soda lime in the metabolic chamber, relative hu- midity was probably low; heat death would probably occur at an even lower temperature under humid conditions in which cooling by evaporation would be limited. A< NOT H OW UDODLED ~ fo) THREE MICE HUDOLED mo Ww f GH DN AN DO OO OXYGEN CONSUMPTION (CC/G/HR) 0 4 a) 12 6 155 ered body temperature. Inclusion of these low values causes the apparent de- crease of the slope of the two curves be- tween 12° and 1°. No body temperatures, however, dropped to the torpid level. Reithrodontomys megalotis is able to main- tain its temperature well above the tor- pid level even when sleeping in cold sur- 20 24 28 32 36 TEMPERATURE °C I'ic. 2.—The rate of oxygen consumption of resting harvest mice at different temperatures in a nest, without nest, and without fur. All three curves have been adjusted, on the basis of the regression lines shown in Fig. 1, to represent a 9-gram mouse. Triangles indicate rate of oxygen consumption of three mice huddled together without a nest compared with the expected rate for the same three mice singly (average weight 8.5 grams). I am grateful to Martin Murie for supplying the value for deep body temperature, which was the average of many determinations made during the day and night at ambient temperatures between 14° and 27°C. The increase in rate of metabolism at cool temperatures is almost linear be- tween 33° and 12°; each drop of 1°C. causes an increase in the rate of oxygen consumption of 0.27 cc/g/hr. This rate of change, possibly because of the small size of harvest mice, is greater than that of any of the rodents listed by Morrison and Ryser (1951) and by Dawson (1955). The averages used for the two points at 1° C. include several low values obtained while the animals probably had a slightly low- roundings. In this respect it differs from the pocket mouse (Perognathus longt- membris), a mouse with which it should be compared because of its similarly small size. When pocket mice are caged at cold temperatures with adequate food, they either drop into torpor or are continually awake and active. They may even be unable to maintain a high body temperature during a prolonged period of sleep at cool temperatures (Bartholo- mew and Cade, 1957). 195 156 OLIVER P. The only other report on the rate of oxygen consumption of harvest mice lists a rate of 3.8 cc/g/hr at 24° C. for mice with an average weight of 9.6 grams (Pearson, 1948a). This rate is almost 10 per cent Jower than the comparable rate obtained from Figure 1 and is below the range of variation obtained at this tem- perature. The difference may be ac- counted for by the fact that the mice used in the earlier study were acclimated to a warmer tempcrature (for discussion of the effect of acclimatization on me- tabolism see Hart, 1957). INSULATING EFFECTIVENESS OF FUR Figure 2 shows also the metabolic et- fect of removing all the fur (277 mg. in fe) CC/G/HR ~ - . oO 7 DM © IZ. 3 2° 3 4 5 eA 9G) Ss) 10 =I \y pe) | VA -: ee Nee PEARSON cent at intermediate temperatures and 24 per cent at 1° C. (lowest curve in Fig. 2). To obtain these measurements, individ- ual mice placed in the metabolic chamber were provided with a harvest mouse nest collected from the wild (shredded grass and down from Compositae), and this the mouse quickly rebuilt into an almost- complete hollow sphere about three inches in diameter. Metabolic rates were counted only when a mouse was resting quictly deep in the nest. THERMAL ECONOMY OF HUDDLING The metabolic economy of huddling was measured on one occasion with three mice at an environmental temperature of 1° C. without nesting material. The rate a SW) ae nes } Re ay. la’ {2 4 2 364 S 6 7 8 ~S -A00 Ul 2 Fic. 3.—Rate of oxygen consumption of a 9-gram harvest mouse for 24 hours at 12°C. the single 8.8-gram specimen used) with an electric clipper. When calculating the points for the curve in [igure 2, 0.28 grams was added to the naked weight and then this rate was adjusted to that for a 9-gram animal on the basis of the regression lines shown in I*igure 1. The rate of metabolism of the naked mouse was about 35 per cent higher at each of the temperatures used, and the rate in- creased 0.38 cc/g/hr for each 1° C. drop in air temperature. INSULATING EFFECTIVENESS OF NESTS When normal, fully furred mice were given an opportunity to increase their in- sulation by constructing nests, their met- abolic rates were lowered about 17 per of metabolism per gram of huddled mice was 28 per cent less than it would have been for a single one of the mice (Fig. 2). The metabolic saving would probably be greater when more mice were huddled to- gether and less when only two mice were huddled, as is true for feral Mus (Pear- son, 1947) and laboratory mice (Prychod- ko, 1958). 24-HOUR OXYGEN CONSUMPTION IN CAPTIVITY Vigure 3 illustrates the rate of oxygen consumption of a mouse kept in the ap- paratus at 12° C. without nesting mate- rial but with food and water for 24 hours. The mouse consumed 1,831 cc. of oxygen to give an average rate of 8.48 cc/g/hr. This is equal to a heat production ot 196 METABOLISM OF HARVEST MICE about 8.8 Calories per day. In agreement with the fact that activity of harvest mice in the wild is greatest shortly after dusk (Pearson, 1969), the oxygen con- sumption was greatest at that time. The prolonged low period lasting from about 8:30 to 10:09 p.m. was unexpected in this nocturnal animal. Pearson (1947) used as an indicator of the nocturnality of different species the ratio of the total amount of oxygen con- sumed at might (60:09 P.M. to 6:00 A.M.) to that consumed in the daytime. For the harvest mouse described in igure 3, the ratio is low--1.02-—but it should be pointed out that the record was made at 12° C., which is colder than the tempera- ture used for the species in the earlier re- port. Temperature atfects the night, day ratio of oxygen consumption because the difference in amount of oxygen con- 157 sumed during rest and during activity is proportionately great at warm tempera- tures and small at cold temperatures. EFFECT OF ACTIVITY ON METABOLISM An athlete is able, for short periods, to raise his rate of metabolism to a level 15 to 20 times his basal rate, but small mammals do not match this effort. The peak metabolic effort of mice running in a wheel is only 6 to 8 times their basal rate (Hart, 1950). At 0° C. lemmings run- ning in a wheel at a speed of 15 em/sec increase their oxygen consumption less than 35 per cent above the level of rest- ing lemmings (Hart and Heroux, 1955). At cool ambient temperatures, such as this, small mammals expend so much energy at rest that a considerable amount of activity causes only a proportionately small increase in oxygen consumption ; TABLE 1 TH 24 HOUR ONYGEN CONSUMPTION (IN C¢ .) OF A 9-GRAM HARVEST MOUSE DURING DECEMBER AND JUNE AT ORINDA, CALIFORNIA DeCEMBER JUNE With With With- Under- With- Undet- out ground out ground Nest Nest Nest Nest Noctur- nal habit 4 hr. above ground 367 367 4 hr. above ground 297 297 ale ihe (Coe at 12-1C7i 20 hr. under ground ~=1,548 1,296 20 hr. under ground = 1,152 954 at OPC. T at 18° C.§ Activily correction | +119 +119 Activity correction | +119 +119 2,034 1,782 cc. 1,568 les 7OFGG; (8.55 Cal.) #4 (6.58 Cal.) # Diurnal habit 20 hr. under ground — 1,548 1,296 20 hr. under ground — 1,152 954 ae Om Cat at 18° C.§ 4 hr. above ground 333 333 4 hr. above ground 155 155 Eke Or (On at 25°C. 77 Activity correction | +119 +119 Activity correction | +119 +119 2,000 1,748 cc. 1,426 12 281CCe (8.39 Cal.)# (5.89 Cal.)# * Mean temperature in runways at time of passage of harvest mice in December. t Mean temperature in runways at time of passage of harvest mice in June. ; Underground temperature in December. § Underground temperature in June. || Add 40 per cent of the oxygen consumption on the surface at a temperature of 12°C. / \ssumed 4.8 Cal. per liter of oxygen. Mean half-hourly temperature in runways between 6 A.M. and 6 P.M. in December. tf Mean half-hourly temperature in runways between 6 A.M. and 6 P.M. in June. 197 158 OLIVER P. and at cold temperatures the metabolic cost of keeping warm may be so high as to leave little or no capacity tor exercise (Hart, 1953). During measurement of the resting metabolism of harvest mice, nu- merous measuring periods had to be dis- carded because the mouse was moving around in the metabolism chamber. Such activity rarely raised the oxygen con- sumption more than 40 per cent above the level of a resting animal at the same temperature. During the 24-hour run at 12°C., the highest metabolic rate oc- curred during an 11-minute period when the average oxygen consumption was 10.36 cc/g/hr. This is only 40 per cent greater than the lowest rate recorded for that mouse during any one measuring period. The maximum metabolic effort recorded for any harvest mouse was that of an 8.6-gram mouse at 1° C. This ani- mal persisted in gnawing, exploring, and trying to escape from the chamber for more than two hours. During one 10-min- ute period its oxygen consumption aver- aged 15.8 cc/g/hr, which is 50 per cent higher than the rate of a resting mouse at the same air temperature and six times the minimum value for the species at thermal neutrality. This is probably not far from the peak metabolic effort of the species. On several occasions I have watched undisturbed harvest mice carrying on their normal activities in the wild, and I have been impressed by their leisurely approach to life. Hard physical labor and strenuous exercise must occur quite in- frequently. Most normal activities of harvest mice are probably accomplished without a rise in metabolic rate more than 50 per cent above what it would be in a resting animal at the same air tem- perature. PEARSON 24-HOUR METABOLISM IN THE FIELD The preceding observations indicate that ambient temperature is a much more important variable than activity in the 24-hour energy budget of harvest mice in the wild. By use of automatic de- vices that record the temperature in mouse runways whenever a mouse passes by, the temperature encountered by har- vest mice during their nightly periods of activity are known (Pearson, 1960). I have also recorded throughout the year the temperature five inches below the surface of the ground. This gives an ap- proximation of the temperature encoun- tered by the mice while they are in their retreats during the daytime. Some of these surface and underground tempera- ture measurements have been used in the calculations summarized in Table 1. To complete the calculations in Table 1, it has been necessary to estimate how many hours of each 24 the mouse spends on the surface of the ground and how many below the surface. No good data exist, so I have made an estimate based on the behavior of captive animals and on automatic recordings made at the exit of an underground nest box being used by wild harvest mice. Admittedly this esti- mate (4 hours on the surface each night) could be wrong by 50 per cent or more, but it should be noted that an error of two hours in this estimate would only alter the answer (the total 24-hour me- tabolism) by about 25 per cent. Assum- ing that the rate of oxygen consumption during above-ground activity is 40 per cent higher than the rate of a mouse rest- ing at 12°C. (see above), the activity correction used in Table 1 can be calcu- Jated. ln 24 hours in December a harvest mouse uses 8.55 Calories, and in June, 6.58 Calories (Table 1), assuming that 198 METABOLISM OF HARVEST MICE the mouse has the benefit of a nest. A nest reduces his daily energy budget by about 12 per cent. These estimates of daily metabolic demands seem reason- able when compared with the values ac- tually obtained by measuring the 24-hour oxygen consumption of captive animals, as reported above. The average metabol- ic impact, or daily degradation of en- ergy, by a single harvest mouse should be somewhere between that in December and that in June, perhaps 7.6 Calories. This is about the same as that of a hum- mingbird in the wild (Pearson, 1954)— less than half that of a much heavier English sparrow (Davis, 1955). BIOENERGETICS In seasons when harvest mice are abun- dant, there may be twelve of them per acre (Brant, 1953). At that population density, the species would be dissipating at the rate of 91 Calories per acre per day the solar energy captured by photosyn- thesis, or something like 3 of 1 per cent of the energy stored each day by the plants in good harvest-mouse habitat in the Orinda area. This percentage was cal- culated using a net productivity of 20,000 Cal/acre/day, which was esti- mated by assuming 4 Calories per gram of dry vegetation (based on data in Brody, 1945, pp. 35, 788) and an annual crop of 1,800 kg. of dry vegetation per acre (based on Bentley and Talbot, 1951). The harvest mice on this hypothetical acre are causing about the same caloric drain on the environment as all the small mammals in the acre of forest described by Pearson (19480). By using caloric units, direct compari- son can be made of the metabolic impact of different species, as in the example above. Similarly, the metabolic cost of different activities and different habits can be compared (Pearson, 1954). For 159 example, harvest mice are strongly noc- turnal (Pearson, 1960), in spite of the fact that air temperatures are much colder at night and force mice to con- sume more oxygen and more food than if they were diurnal. Since evolution has permitted nocturnality to persist, it seems logical to assume that the value of nocturnality to harvest mice is greater than the metabolic cost. I estimate that during a 24-hour period in December a 9-gram harvest mouse uses 0.16 more Calories by being nocturnal than it would if it were diurnal (Table 1). In summer, the difference is even greater, 0.69 Calories. The average is 0.42 Cal- ories, or about 34 grains of wheat. This is a rough estimate of the price each har- vest mouse pays for nocturnality. Some environmental pressure makes harvest mice remain nocturnal, and this pressure must be more than 0.42 Calories per mouse per day. If harvest-mouse noc- turnality evolved for one reason only—to avoid predation by hawks—then we would have discovered a minimum esti- mate of the predation pressure of hawks on harvest mice. Surely the situation is not this simple; nevertheless, it is inter- esting to measure the pressure that makes harvest mice nocturnal even if the cause of the pressure is not known. SUMMARY Oxygen consumption of harvest mice reaches a minimum of 2.5 cc/g/hr at an ambient temperature of 33° C., and the zone of thermal neutrality is not more than 3°. Each drop of 1° in ambient tem- perature causes an increase in the rate of metabolism of 0.27 cc/g/hr. Removing the fur raises the rate of metabolism about 35 per cent, and use of a nest lowers it 17 to 24 per cent. Huddling by three mice at 1° reduces the rate 28 per cent. 199 160 OLIVER P. I-xercise at cool temperatures causes a relatively small increase in the rate of metabolism, whereas change ot ambient temperature has a great effect. Making use of the temperatures that harvest mice are known to encounter in the wild, the 24-hour oxygen consumption of a wild harvest mouse was calculated to be 1,782 cc. in December and 1,370 cc. in June. The average (1,576 cc.) is equivalent to PEARSON about 7.6 Calories per day. A dense pop- ulation of harvest mice would dissipate about 91 Calories per day per acre, which is about 4 of 1 per cent of the energy stored by the plants each day. By being nocturnal, harvest mice en- counter cooler temperatures, and this habit increases the ‘daily energy budget of each mouse by 0.42 Calories, or about 3 grains of wheat. LITERATURE CITED BaRTHOLOMEW, G. A., and Cape, T. J. 1957. Tem- perature regulation, hibernation, and aestivation in the little pocket mouse, Perognathus longimem- bris. Jour. Mammal., 38:60-72. BENTLEY, J. R., and TaLBot, M. W. 1951. Efficient use of annual plants on cattle ranges in the California foothills. U.S. Dept. Agriculture, Cir- cular No. 870, 52 pp. Brant, D. H. 1953. Small mammal populations near Berkeley, California: Reithrodontomys, Peromys- cus, Microtus. Doctoral thesis, University of Cali- fornia, Berkeley. Bropy, S. B. 1945. Bioenergetics and growth. New York: Reinhold Publishing Corp. Davis, E. A., JR. 1955. Seasonal changes in the energy balance of the English Sparrow. Auk, 72:385-411. Dawson, W. R. 1955. The relation of oxygen con- sumption to temperature in desert rodents. Jour. Mammal., 36:543-53. Dr Bont, A.-F. 1945. Métabolisme de repos de quelques espéces d’oiseaux. Ann. Soc. Roy. Zodl. Belgique, 75 (1944) :75-80. Hart, J. S. 1950. Interrelations of daily metabolic cycle, activity, and environmental temperature of mice. Canadian Jour. Research, D, 28:293- 307. ———. 1953. The influence of therma] acclimation on limitation of running activity by cold in deer mice. Canadian Jour. Zodl., 31:117-20. . 1957. Climatic and temperature induced changes in the energetics of homeotherms. Revue Canadienne de biol., 16:133-74. Hart, J. S., and Heroux, O. 1955. Exercise and temperature regulation in lemmings and rabbits. Canadian Jour. Biochem. & Physiol., 33:428-35. Morrison, P. R. 1947. An automatic apparatus for the determination of oxygen consumption, Jour. Biol. Chem., 169:667-79. Morrison, P. R., and Ryser, F. A. 1951. Tempera- ture and metabolism in some Wisconsin mam- mals. Federation Proc., 10:93-94. ———. 1959. Body temperature in the white-footed mouse, Peromyscus leucopus noveboracensis. Phys- iol. Zodl., 32:90-103. PEARSON, O. P. 1947. The rate of metabolism of some small mammals. Ecology, 28:127-45. . 19484. Metabolism of small mammals, with remarks on the lower limit of mammalian size. Science, 108:44. ———. 1948). Metabolism and bioenergetics. Sci- entific Monthly, 66:131-34. . 1954. The daily energy requirements of a wild Anna Hummingbird. Condor, 56:317-22. . 1960. Habits of harvest mice revealed by automatic photographic recorders. Jour. Mam- mal. (in press). PryYCHODKO, W. 1958. Effect of aggregation of labo- ratory mice (Mus musculus) on food intake at different temperatures. Ecology, 39:500-503. Reprinted for private circulation from PHYSIOLOGICAL ZOOLOGY Vol. XX XIII, No. 2, April 1960 Copyright 1960 by the University of Chicago 200 OXYGEN CONSUMPTION, ESTIVATION, AND HIBERNATION IN THE KANGAROO MOUSE, MICRODIPODOPS PALLIDUS! GEORGE A. BARTHOLOMEW AND RICHARD E. MacMILLEN Departments of Zodlogy, University of California, Los Angeles, and Pomona College, Claremont, California HE pallid kangaroo mouse occurs | only in the desert parts of western Nevada and extreme eastern Cali- fornia. Its habitat is restricted to areas of fine sand which support some plant growth. Like its relatives, the kangaroo rats (Dipodomys) and the pocket mice (Perognathus), it is nocturnal, fossorial, and gramnivorous and can under some circumstances live indefinitely on a dry diet without drinking water. The genera] life history (Hall and Linsdale, 1929) of this kangaroo mouse and the details of its distribution (Hall, 1946) are known, but virtually no quantitative data on its physiology are available. The present study was undertaken to compare the thermoregulation of Mzcro- dipodops with that of the better-known genera, Dipodomys and Perognathus. These three genera belong to the family Heteromyidae, which has been more suc- cessful in occupying the arid parts of western North America than any other group of mammals. 1 This study was aided in part by a contract be- MATERIAL AND METHODS Experimental animals——The twenty- three kangaroo mice used were trapped in sand dunes four miles south of Arle- mont Ranch, Esmeralda County, Neva- da, in April, 1959, and May, 1960. They were housed individually in small ter- rarija partly filled with fine sand, kept ina windowless room on a photoperiod of 12 hours, and fed on a diet of mixed bird seed supplemented occasionally with small pieces of cabbage. Survival was excellent, and some of the animals were kept for over ten months. Body temperatures-—All temperatures were measured with 30-gauge copper- constantan thermocouples connected to a recording potentiometer. All body tem- peratures were taken orally by inserting a thermocouple to a depth of at least 2 cm. Ambient temperatures——The ambient temperatures were monitored with ther- mocouples and controlled by insulated chambers equipped with automatic heat- ing and cooling units, blowers, and tween the Office of Naval Research, Department of lizhts the Navy, and the University of California (Nonr eles ; 266[31)). Oxygen consumption—Oxygen con- Liver 201 178 sumption was measured by placing a mouse in an air-tight 500-cc. glass con- tainer equipped with a thermocouple and ports for the introduction and removal of air. The bottom of the container was covered to a depth of about 1 cm. with fine dry sand. The glass container with animal inside was placed in a tempera- ture-control chamber, and dry air was metered through the container at a rate og © BODY TEMP. GEORGE A. BARTHOLOMEW AND RICHARD E. MacMILLEN the response of body temperature (Tz) to moderately low ambient temperatures (T4), kangaroo mice were placed at T4 of 7°—-9° C. for five days starting May 11, 1959, with tood available in excess; measurements of 7, were made at 24- hour intervals. There were no apparent changes in 7, during the test period, nor was the mean 7, significantly different from that of animals maintained at room C oO ° af Te) me) als L~ rm oO ° s oO T+ | ww N ine) Fic. 1.—Body temperatures of M. pallidus at various ambient temperatures. A, 47 measurements on twelve animals; B, 38 measurements on thirteen animals; C, 7 measurements on four animals; D, 9 measure- ments on four animals (three other animals tested at this temperature died). The horizontal lines indicate the means (M). The rectangles inclose M + oy. The vertical lines indicate the range. of 250 cc/min and then delivered to a Beckman paramagnetic oxygen analyzer which, used in conjunction with a re- cording potentiometer, gave a continu- ous record of oxygen consumption. All data used were from _ post-absorptive animals. RESULTS Body temperature during normal ac- tivity —Normally active animals kept at room temperature (22.4°-25.4° C.) had body temperatures ranging from slightly less than 37° to as high as 41° C., with a mean of 38.8° C. (Fig. 1). To determine temperature. The animals appeared nor- mally active and unaffected by the change in environmental temperature. Animals were maintained at 7,4 of 37.5°-40.5° C. for 24 hours to test their response to moderately high environ- mental temperatures. They showed a conspicuous elevation in 7 with a mean almost 2° C. higher than that of animals at room temperature. Animals main- tained at T4 close to 35° C. also became hyperthermic and showed a mean TY; in- termediate between that of animals held at room temperatures and those held at 39° C. There was no mortality in animals 202 THERMOREGULATION IN held at 35° C., but exposure to 39° C. for more than a few hours killed three out of the seven animals tested. At a high T4 the kangaroo mice did not salivate or pant; they merely sprawled out flat on the sand with legs extended and lower jaw and neck prone on the substrate. This prone posture alternated with brief bursts of intense activity characterized by repeated shifts in position and much digging and moving of sand. CC. Oo /GM./HR. 10 20 THE KANGAROO MOUSE 179 gm.) is 1.8 cc O2/gm/hr when the for- mula M = 3.8W-°7 is used (see Brody, 1945, and Morrison, Ryser, and Dawe, 1959). The observed basal metabolism of our kangaroo mice (mean, 1.3 + 0.2 cc O./gm/hr) was about three-fourths of the predicted value. This relatively low figure is consistent with the obser- vation on some other heteromyids (Daw- son, 1955). The only comparative data on the 4 30 40 °C Fic. 2.—The relation of oxygen consumption to ambient temperature. Data obtained from ten animals. Each point represents the minimum level of oxygen consumption maintained by an animal for half an hour. Oxygen volumes are corrected to 0° C. and 760 mm. (Hg.) pressure. Oxygen consumption —The relation of oxygen consumption to 74 is summarized in Figure 2. There is no clearly defined zone of thermal neutrality, but oxygen consumption is minimal at about 35° C. The increase in oxygen consumption at temperatures above 35°C. is relatively more rapid than is the increase below this point of thermal neutrality. No dif- ferences in oxygen consumption were ap- parent between males and females. The calculated metabolism of Micro- dipodops pallidus (mean weight, 15.2 energy metabolism of Microdipodops is that of Pearson (1948) on M. megacepha- lus. Pearson’s data, obtained at tempera- tures near 24° C. from animals that were not post-absorptive, gave oxygen con- sumptions of 3.4~3.7 cc O2/gm/hr. Pear- son’s measurements, as might be expect- ed from the fact that he was not using post-absorptive animals, are higher than our determinations of 2.7 cc O2/gm/hr ab ZS °C. Hibernation and estivation—No infor- 203 180 mation on hibernation or estivation is available for Microdipodops. Hall (1946, p. 386) pointed out that kangaroo mice are often active above ground in temper- atures many degrees below freezing, and Ingles (1954, p. 214) suggested that kangaroo mice probably do not hiber- nate. Under laboratory conditions we found that kangaroo mice at any time of year °C BODY TEMP. 10 20 30 MINUTES FROM GEORGE A. BARTHOLOMEW AND RICHARD E. MacMILLEN there are no conspicuous physiological differences between arousal from spon- taneous dormancy and that from induced dormancy. Animals dormant at room tempera- tures (estivating) started to arouse im- mediately upon being handled. The rate of increase in Tz varied but usually fell between 0.5° and 0.8°C. per minute. Usually within 20 minutes of the onset 40 30 20 50 START OF AROUSAL 40 60 Fic. 3.—Increases in oral temperatures in nine kangaroo mice during arousal from torpor. All arousals took place in ambient temperatures between 23° and 26° C. Temperatures taken manually with thermo- couples. The five upper animals were dormant at room temperature (22°-25° C.); the four lower animals were dormant at 5°-8° C. will spontaneously become dormant at ambient temperatures ranging at least from 5° to 26° C. and can readily be in- duced to hibernate (or estivate) over this range of temperatures by reduction of food for 24 hours or less. Body temperature and behavior dur- ing entry into torpor were not recorded, but the animals apparently entered tor- por in the crouching posture normally used in sleeping. Dormant animals had body temperatures 1°-2° C. above am- bient. Judging from the course of body temperature during arousal from torpor, of arousa! the animals attained their nor- mal operating temperature, and within as little as 12-15 minutes from the start of arousal they appeared to behave nor- mally, even though 7, approximated 30° C. Arousal from low temperatures was essentially the same as arousal from high temperatures (Fig. 3). However, animals arousing from low temperatures attained maximal body temperatures about 1° C. higher than did those arous- ing from room temperature. Incidental to the measurement of Ts, the relations of various types of behavior 204 THERMOREGULATION IN THE KANGAROO MOUSE to body temperature were noted during nine arousals. Mice unsuccessfully at- tempted to right themselves when turned over at Ts between 16.1° and 18.2°C. and successfully righted themselves at Tp between 19.0° and 22.0° C. The first vocalizations were given at 7, between 24.7° and 28.6° C. Grain was available to the animals during arousal, and seven of the nine animals ate during arousal. The lowest Ts for eating was 25.5°C., and three animals ate at temperatures between 25° and 29.4° C. The mean Ts for onset of visible shivering for seven animals was 25.5° C. Two of the nine animals observed did not visibly shiver during arousal. Shivering usually stopped at a Tz of 34°-35° C. DISCUSSION The general features of thermoregula- tion in Microdipodops pallidus are similar to those of the related genus Perognathus in that both show well-developed pat- terns of hibernation and estivation, es- sentially normal behavior at T, below 35° C., obligate hyperthermia at Ts above 35° C., and no apparent salivary response to elevated body temperature. Microdipodops differs from the related genus Dipodomys in that the latter does not readily become dormant at either high or low temperatures and does use salivation as an emergency thermoregu- latory response (Schmidt-Nielsen and Schmidt-Nielsen, 1952). In kangaroo mice, as in Perognathus longimembris (Bartholomew and Cade, 1957) and Citellus mohavensis (Bartholo- mew and Hudson, 1960), there appears to be no sharp physiological differentiation between hibernation and estivation. This underscores the point that the faculta- tive hypothermia shown by mammals should not be thought of only as an adap- tive response to low environmental tem- peratures; at least for small desert mam- 181 mals the ability to become dormant and to decrease body temperature and meta- bolic activity may be more useful in the summer than in the winter, and it may be as important for water conservation as for energy conservation. Kangaroo mice are unique among heteromyids in having conspicuous de- posits of adipose tissue in the proximal third of the tail, which is considerably larger than either its base or its distal half. Hall (1946, p. 379) suggests that the fleshiness of the tail permits it to func- tion in balancing. However, since these mice hibernate but do not show conspicu- ous seasonal deposits of subcutaneous fat over the body as a whole, it seems reason- able to suggest that the fat tail serves as a reserve of energy for use during periods of torpor. In the laboratory with food available in excess, many of the kangaroo mice showed a marked increase in tail diameter. Our data (Fig. 1) show almost no in- dication of a discrete zone of thermal neutrality for the kangaroo mouse. Its critical temperature is unusually high for an animal living in an area characterized by cold winters. For months on end kan- garoo mice can be active only at tempera- tures below thermal neutrality. Presum- ably, their energetic and thermal prob- lems are reduced in cold weather by pe- riodic episodes of torpor. It is of interest that we captured our animals on nights when environmental temperatures went below —10° C., and Hall (1946, p. 396) reports that these animals are often “‘ac- tive on nights when the temperature is so low as to freeze to a state of stiffness the bodies of mice caught in traps.”’ Thus, al- though they can hibernate, they are also commonly active during subfreezing weather. This species has remarkably shallow burrows, often no deeper than 4 inches (Hall, 1946, p. 396). Consequently, when 205 182 high daytime temperatures occur, at least some members of the population may be exposed to temperatures near 35° C. It is possible, therefore, that the high point of thermal neutrality of this species allows a significant metabolic economy and a significant reduction in pulmocutaneous water loss during the severely hot desert summers. Extrapolation of the plot of metabo- lism against ambient temperature below thermal neutrality does not intersect the abscissa within the usual range of body temperature (38°-39°C.) of kangaroo mice (Fig. 2). This means that, unlike some of the species considered by Scho- lander et al. (1950), and unlike the masked shrew, Sorex cinereus (Morrison, Ryser, and Dawe, 1959), the kangaroo mouse does not follow Newton’s empiri- cal law of cooling in a simple and direct manner. The failure to follow the pattern predicted by Newton’s law of cooling may be related to the fact that kangaroo mice start to become hyperthermic as they approach their critical temperature (Fig. 1), and it suggests that the relation between skin and ambient temperature in this species differs from the usual pat- tern. It is of interest that Pearson’s data (1960) for Reithrodontomys show a situa- tion similar to that reported here for Microdipodops, that is, almost no zone of thermal neutrality, a high critical tem- perature, and a failure of the curve of metabolism against ambient temperature to intersect the abscissa at the usual body temperature. Although Pearson does not comment on this point, it appears that in Reithrodontomys as in Microdipodops the curve of metabolism against ambient temperature intersects the abscissa at a point above the lethal temperature for the species. The apparent absence of a marked in- crease in salivation at high temperatures GEORGE A. BARTHOLOMEW AND RICHARD E. MacMILLEN in Microdipodops correlates nicely with its strong tendency toward hyperthermia at high ambient temperatures. For ani- mals living in a desert environment where water is usually in short supply, hyperthermia is a more advantageous re- sponse to heat than is evaporative cool- ing. SUMMARY Microdipodops pallidus occurs only on sparsely vegetated sand dunes in the desert parts of western Nevada and eastern California. In the absence of temperature stress body temperature, Tp, averages 38.8°C. There is no diminu- tion of Tz with decreasing ambient tem- perature, T4, at least to 8° C. However, hyperthermia is apparent at a Ty, of 35° C. and at 39° C. Tz averages 40.5° C. Exposure for more than a few hours to 39° C. is often lethal. At high ambient temperatures kangaroo mice neither pant nor drool. They have no clearly de- fined zone of thermal neutrality; oxygen consumption is minimal at 35° C. and in- creases more rapidly at temperatures above this point than below it. Basal metabolism is 25 per cent less than that predicted on the basis of body size. Kan- garoo mice are capable of both estivation and hibernation. In the laboratory they often become dormant at ambient tem- peratures ranging at least from 5° to 26° C. The rate of temperature increase during arousal at room temperature is 0.5°-0.8° C. per minute. Terminal body temperatures after arousal from low tem- peratures averaged about 1° C. higher than after arousal from room tempera- ture. By the time the 7 of arousing ani- mals reaches 30° C., their behavior ap- pears normal. The thermoregulatory re- sponses of kangaroo mice are compared with those of other desert heteromyids, and the ecological significance of their physiological capacities is discussed. 206 THERMOREGULATION IN THE KANGAROO MOUSE 183 LITERATURE CITED BARTHOLOMEW, G. A., and Cang, T. J. 1957. Tem- perature regulation, hibernation, and aestivation in the little pocket mouse, Perognathus longimem- bris. Jour. Mamm., 38:60-72. BaRTHOLOMEW, G. A., and Hupson, J. W. 1960. Aestivation in the Mohave ground squirrel, Citel- lus mohavensis. Bull. Mus. Comp. Zool., 124:193- 208. Bropy, S. 1945. Bioenergetics and growth. New York: Reinhold Publishing Co. Dawson, W. R. 1955. The relation of oxygen con- sumption to temperature in desert rodents. Jour. Mamm., 36:543-53. INGLES, L. G. 1954. Mammals of California and its coastal waters. Stanford, Calif.: Stanford Univer- sity Press. Hatt, E. R. 1946. Mammals of Nevada. Berkeley: University California Press. Hatt, E. R., and Lrnspateg, J. M. 1929. Notes on the life history of the kangaroo mouse (Microdz- podops). Jour. Mamm., 10:298-305. Lyman, C. P., and CHATFIELD, P. O. 1955. Physiol- ogy of hibernation in mammals. Physiol. Rev., 35:403-25. Morrison, P., Ryser, F. A., and Dawe, A. R. 1959. Studies on the physiology of the masked shrew Sorex cinereus. Physiol. Zoél., 32:256-71. PEARSON, O. P. 1948. Metabolism of small mam- mals, with remarks on the lower limit of mam- malian size. Science, 108:44. . 1960. The oxygen consumption and bio- energetics of harvest mice. Physiol. Zodl., 33: 152-60. ScHMmipT-NIELSEN, K., and Scumipt-NIELSEN, B. 1952. Water metabolism of desert mammals. Physiol. Rev., 32:135-66. SCHOLANDER, P. F., Hock, R., WALTERS, V., JOHN- SON, F., and Irvine, L. 1950. Heat regulation in some arctic and tropical mammals and birds. Biol. Bull., 99:237-58. Reprinted for private circulation from PHYSIOLOGICAL ZOOLOGY Vol. XXXIV, No. 3, July 1961 Copyright 1961 by the University of Chicago PRINTED IN U.S.A. 207 Counter-Current Vascular Heat Exchange in the Fins of Whales’ P. F. SCHOLANDER anp WILLIAM E. SCHEVILL. From the Woods Hole Oceanographic Institution, Woods Hole, Massachusetts T MAY BE a Source of wonder that whales swimming about in the icy waters of the polar seas can maintain a normal mam- malian body temperature. What prevents them from being chilled to death from heat loss through their large thin fins?? These are well enough vascularized to justify the question (fig. 1). One may conjecture that a whale may be so well insulated by its blubber that it needs such large surfaces to dissipate its heat. On the other hand, if heat conservation is at a pre- mium, there must be some mechanism whereby the fins can be circulated without losing much heat to the water. One may point to two circulatory factors which would reduce the heat loss from the fin: a) slow rate of blood flow and, 6) precooling of the arterial blood by veins before it enters the fin. Bazett and his coworkers (1) found that in man the brachial artery could lose as much as 3°C/decimeter to the two venae comitantes. This simple counter-current exchange system is a mere rudiment compared to the multi- channelled arteriovenous blood vascular bun- dles which we find at the base of the extremities in a variety of aquatic and terrestrial mammals and birds. These long recognized structures have most recently been studied by Wislocki (2), Wislocki and Straus (3) and Fawcett (4). The function of these bundles has long been a mystery. No matter what else they do, they must exchange heat between the arteries and veins, and it has been pointed out that they very likely play an important role in the pres- ervation and regulation of the body heat of many mammals and birds (5). In the present study we describe a conspic- uous arteriovenous counter-current system in the fins and flukes of whales, which we interpret as organs for heat preservation. Received for publication July 21, 1955. 1 Contribution Number 807 from the Woods Hole Oceanographic Institution. 2Tn ‘fin’ we include the structures more specifically called flippers (pectoral fins), flukes (caudal fins) and dorsal fin. MATERIAL Two species of porpoises have been studied: Lageno- rhynchus acutus: dorsal fin, tail-fluke, and flipper of an adult female collected 50 miles east of Cape Cod; Tursiops truncatus: dorsal fin and tail-fluke of a 4- month-old calf from Florida, supplied through the courtesy of the Marineland Research Laboratory. Lagenorhynchus is a genus of fairly high latitudes, the southern limit of L. acutws being about latitude 41°N. on the New England coast and about 55°N. in the British Isles. It has been caught at least as far north as latitude 64°N. in west Greenland and Nor- wegian waters. Tursiops is found in lower latitudes, T. truncatus overlapping slightly with ZL. acutus and occurring south into the tropics. DESCRIPTION Figure 2 illustrates the vascular supply at the base of the dorsal, pectoral and caudal fins. It may be seen that all major arteries are located centrally within a trabeculate venous channel. This results in two concentric con- duits, with the warm one inside. In addition to the circumarterial venous channels there are separate superficial veins, as seen in figure 2. The circumarterial venous channels are con- spicuously thin walled compared to the simple veins, aS may be seen in figure 3. When an artery was perfused with saline, the solution returned through both of these venous systems. INTERPRETATION Based on the anatomical findings and on the perfusion experiments, we interpret the artery- within-vein arrangement as a heat-conserving counter-current system, as schematically pre- sented in fig. 4. In such an arrangement the warm arterial blood is cooled by the venous blood which has been chilled in the fin. The result is a steep proximodistal temperature drop from the body into the appendage. The heat of the arterial blood does not reach the fin, but is short-circuited back into the body in the venous system. Body heat is therefore conserved at the expense of keeping the appen- dage cold. There is reason to believe that the analogous blood vascular bundle in the proxi- 279 208 Gq I'ic. 1. Arterial supply to the flukes in the common porpoise (Phocoena phocoena), drawn from an X-ray picture by Braun (6). mal part of the extremities of sloths serves a similar function, inasmuch as these animals can barely keep warm even in their warm environment (5). Cold extremities have been described in many arctic mammals and birds as important factors for conservation of body heat (7), but to what extent arteriovenous counter-current structures are present in these animals is not known. The efficiency of heat exchange in a system like that diagrammed in figure 4 is related to the blood flow. The slower the flow, the more nearly identical will be the arterial and venous temperatures along the system, and the more efficient will be the heat conservation. At high rates of flow, warm blood will reach the periph- L. CAUDAL DORSAL SSeS O CENTIMETERS AS R. CAUDAL LAGENORHYNCHUS ACUTUS P. F. SCHOLANDER AND WILLIAM E. SCHEVILL Volume 8 ery and cool venous blood will penetrate into the body.’ It was shown by perfusion experiments on the detached fins that the arterial blood may return via the concentric veins, and/or through the separate superficial veins. As pointed out above, the concentric vein channels are very thin walled and weak compared to the thick- walled superficial veins (fig. 3). One may inter- pret these anatomical facts in the following way. If the animal needs maximal heat con- servation, blood circulaticn through the fins should be slow, and the venous return should preferentially take place through the counter- current veins. But a slow rate of blood flow would need only weak venous walls, as actually found. If, on the other hand, the animal needed maximal cooling, as during exercise in rela- tively warm water, this would be most effec- tively accomplished by a high rate of blood flow through the fins, with venous return through the superficial veins and the least possible flow through the concentric veins. This would require the strong and thick walls of the superficial veins. One may even see the likelihood of a semiautomatic regulatory func- tion in the concentric system, for when the artery is swelled by increased blood flow, the concentric veins will be more or less obliterated, 3 The theory for a multichannel counter-current systern has been elaborated in connection with the swimbladder in deep sea fishes (8). Tic. 2. Sections near base of fins and flukes of two species of porpoises. Fach artery is sur- rounded by a multiple venous channel. Simple veins are near the skin (only the larger ones are indi- cated). 209 COUNTER-CURRENT HEAT EXCHANGE IN WHALE FINS i ospet te |b dd "oS Laat php weer oe 281 ANG ae one Me ae or ati Wg s Fic. 3. are from Tursiops truncatus. (Courtesy of the Department of Anatomy. Harvard Medical School.) A. From tail-fluke. Upper: artery surrounded by thin-walled venous channels. Lower: superficial single thick- walled vein in the hypodermis. (X 9) B. From dorsal fin. Artery surrounded by thin-walled venous channels (X 12) but will remain open when the diameter of the artery is reduced during decreased blood flow. Thus the anatomical findings fit logically into the simplest possible scheme of heat regulation in the fins. There are a few observations available in- dicative of heat regulation in the fins of por- poises. Tomilin (9) made some observations on an east Siberian ‘white-sided dolphin’ on deck, and found that the fins could vary be- tween 25° and 33.5°C, while the body varied only 0.5°. Schevill observed that the flukes in a Florida Tursiops out of water became about 1o° warmer than the body surface itself. In both of these cases the animals were probably resisting overheating. On the other hand, Scholander (5) has recorded cold flippers in water-borne common porpoises (Phocoena). The concentric counter-current system of an artery within a vein appears to be a pecu- liarly cetacean arrangement, and we have seen it only in the fins, flippers and flukes of these animals.4 This is an impressive example of bioengineering, which, together with other 4The present material is from odontocetes, but these structures have also been noted by Scholander in the tail flukes of a mysticete (fin whale). Fic. 4. Schematic diagram of hypothetical tempera- ture gradients in a concentric counter-current system. factors, adapts these homeotherms for a suc- cessful existence in a heat-hungry environment. SUMMARY The vascular supply to the fins and flukes of two species of porpoises, Lagenorhynchus acutus and Tursiops truncatus, is described. All major arteries entering the fins and flukes 210 982 P. F. SCHOLANDER AND WILLIAM E. SCHEVILL Volume 8 are surrounded by a trabeculate venous chan- nel. The arteries drain into these, but also into 1. superficial simple veins. The artery within the venous channel is interpreted as a heat-con- serving counter-current exchange system. The heat regulatory aspects of the two venous systems are discussed. We wish to express our appreciation to Dr. F. G. Wood, Jr., and the Marineland Research Laboratory, Marineland, Fla., for providing the material of Tur- siops truncatus, and to Dr. G. B. Wislocki of the Dept. of Anatomy, Harvard Medical School, Boston, Mass., for providing the histological sections and photographs. NON Ff ee) REFERENCES Bazett, H. C., L. Lovzt, M. Newron, L. EISEN- BERG, R. Day And R. Forster II. J. Appl. Physiol. 1: 3, 1948. . WistockI, G. B. J. Morphol. 46: 317, 1928. 3. WisLockI, G. B. AND W. L. Straus, Jr. Bull. Mus. Comp. Zool. Harvard 74: 1, 1932. . Fawcett, D. W.J Morphol. 71: 105, 1942. . SCHOLANDER, P. F. Evolution 9: 15, 1955. . Braun, M. Zool. Anz. 29: 145-149, 1905. . Irvinc, L. anp J. Kroc. J. Appl. Physiol. 7: 355, 1955: . SCHOLANDER, P. F. Biol. Bull. 107: 260, 1954. 9. TomiLin, A. G. Rybnoe Khozaistvo 26: 50, 1950. (In Russian.) 211 RE cea aft Tne Tee " tLaiay = CUS - - rey ged a a: iuleye ae WE ; “se 11, obey AF 7 enieta ee eee geepeneh, Oe ivorie wt SECTION 3—REPRODUCTION AND DEVELOPMENT Just as animal structures must be adaptive, so must reproductive and de- velopmental patterns; the organism must be a functioning unit in its environ- ment at all stages of its life cycle. In our selections, Millar discusses the evolu- tion of litter size, and Sharman points out the adaptive value of some peculiari- ties of kangaroo reproduction. The interrelationships of reproductive and developmental patterns in the fisher are evident in the account by Wright and Coulter. Superfetation (or the fertilization of new ova during gestation, known in kangaroos, rabbits, and some rodents), delayed implantation (mainly in some mustelids, bears, and pinnipeds), and delayed fertilization (through sperm storage, known in some bats) all are interesting adaptive variations of the reproductive theme. Conaway reviews the adaptive sig- nificance of several reproductive patterns. A study of the reproductive adapta- tions of the red tree vole by Hamilton (1962), not reprinted here, related small litters, long gestation, delayed implantation during lactation, and slow de- velopment of young with the limited amount of energy available in the vole’s food sources. The classic summary of mammalian reproduction by Asdell (as revised in 1964), Sadlier’s monograph (1969) on ecology of reproduction. and collections of contributions edited by Enders (1963) on delayed implanta- tion and by Rowlands (1966) on comparative biology of mammalian reproduc- tion also will repay study. The study of pheromones—chemicals produced by organisms that transmit olfactory signals—is a new and growing area combin- ing reproductive and behavioral biology. Bronson’s review is based mainly on laboratory experiments, but he discussed concepts of obvious importance to the mammalogist who would understand the physiological bases of phenomena such as the Bruce and Whitten effects, and their adaptive significance. Two classic books in the field of development in which relative growth rates were considered at length are On Growth and Form by D’Arcy Went- worth Thompson (1942) and Problems of Relative Growth by Julian Huxley (1932). A detailed account (too long to include here) of one species in terms of relative growth and in comparison to several other species is the study by Lyne and Verhagen (1957) on Trichosurus vulpecula, an Australian brush- tailed possum. Allen’s paper (reprinted here) is of interest because it is one of the earliest to give serious consideration to variation with age and to pos- sible relevance of such variation to systematic and other problems. Hall (1926) described at greater length than could be included here and in detail un- common at that time the changes during growth of the skull in the California ground squirrel. Two among the many good studies of development of single species are by Layne (1960, 1966) on Ochrotomys nuttalli and Peromyscus floridanus. Clark’s study of the Richardson ground squirrel is typical of many short descriptive papers in this area. Although we have not included examples of methods of determining age other than the report of Wright and Coulter on the fisher, we must comment that age determination is important in many practical problems relating to wildlife management as well as in studies of population composition or of growth as such. Managers of deer herds, for example, can examine the teeth of hunter-killed animals using standards developed by Severinghaus (1949) 213 and later workers. Age determination by annuli was reviewed by Klevezal and Kleinenberg (1969)—see Adams and Watkins (1967) on its application to ground squirrels. Epiphyseal growth as observed in X-ray photographs and the use of lens weights are other means (see Wight and Conaway, 1962, on aging cottontails ). A short paper on maturational and seasonal molt in the golden mouse con- cludes our selection for this section. Studies of molt in furbearers are, of course, of special economic import, and knowledge of pelage differences re- lated to age, sex, or season are of obvious use in most studies of mammalian populations. The literature on mammalian reproduction and development is widely scattered. Journals such as GRowTH, DEVELOPMENTAL BioLocy, and BioLocy OF REPRODUCTION contain much of interest to mammalogists, but other jour- nals, either more (e.g., ENDocRINOLOGY) or less (e.g., THE JOURNAL OF Ex- PERIMENTAL ZOOLOGY ) specialized, must also be consulted. 214 EVOLUTION OF LITTER-SIZE IN THE PIKA, OCHOTONA PRINCEPS (RICHARDSON ) Joun S. Mitrart Department of Zoology, University of Alberta, Edmonton, Alberta Received May 30, 1972 Attempts to explain the evolutionary significance of litter-size have been rela- tively few, but varied in approach and scope. Lack (1948) considered that natural selection favors those animals producing the most offspring because they leave the most descendants. He suggested that an “upper limit is set by the number of young which the parents can successfully raise” but recognized that “there is an evolu- tionary alternative between producing more young, or fewer young which are better nourished and better protected.” Several hypotheses have been based on Lack’s basic premise that natural selection favors the production of maximum number of off- spring. These generally view litter-size as only part of an overall reproductive strat- egy, but differ in the parameters considered important in determining litter-size. For example, “resources,” length of breeding season, food supply, body size, altitude, latitude, mortality, population stability, and competition have all been suggested to influence litter-size directly or indirectly (Lord, 1960; Cody, 1966; Gibb, 1968; Smith and McGinnis, 1968; Spencer and Steinhoff, 1968). During a study of the pika Ochotona princeps (Richardson) in southwestern Al- berta, data on reproduction, mortality, and population density were obtained. Here these data are used to evaluate the sig- nificance of litter-size in pikas. Several aspects of the biology of these animals have been reported by Millar (1972a, b) and Millar and Zwickel (1972a, b). 1Present Address: Department of Zoology, University of Western Ontario, London 72, On- tario. EvoLuTIon 27:134-143. March 1973 METHODS A total of 667 animals were collected from several study areas by _ shooting throughout the breeding seasons of 1968, 1969 and 1970. Ovaries of mature females were fixed in A.F.A. (alcohol-formalin, acetic acid), embedded in paraffin, and serially sectioned at 7-10u. Corpora lutea and corpora albicantia were counted microscopically, and these counts were considered to be the litter-size at concep- tion, or potential litter-size. Such counts may be biased by twinning of ova or poly- ovulation. Polyovulation and twinning. of ova would result in females having more embryos than corpora lutea, but this situa- tion was not observed. Twinning of ova would result in some embryos sharing a chorion with another, but again, none were found. Stage of gestation was de- termined from the size of embryos in collected females, and all embryonic losses occurred prior to mid-pregnancy (Millar, 19725). The number of healthy embryos in late gestation was considered to be the litter-size at birth; the difference between the number of corpora lutea and healthy embryos in late stages of pregnancy pro- vided an estimate of prenatal losses. Discrete fat bodies were present in the interscapular, cardiac, and splenic regions of collected animals. These were removed and weighed, and mg fat per 100 gm body wt was used as an index of condition. Age of collected animals was determined from histological sections of lower jaws. Adult mortality rates were based on age structure of the populations (Millar and Zwickel, 1972a). Several marked populations were fol- lowed on one area during the three years 215 EVOLUTION OF LITTER-SIZE IN THE PIKA 135 °e TABLE 1. Litter-size and number of litters per season of North American pikas. Litter-size based on counts of embryos. Litter-size Litters per Region 1 2 i 5 Season Source California 1 6 8 1 3-4 Severaid, 1955 2 3) - Grinnell et al., 1930 Nevada 1 5 - Hall, 1946 Oregon 2k Bailey, 1936 2 - Roest, 1953 Colorado 1 2 1 z Johnson, 1967 2 Anderson, 1959 1y Dice, 1927 3 a Present study Colorado and Utah 3 4 2 Hayward, 1952 Utah 1 - Long, 1940 Washington 1 2t Dice, 1926 British Columbia lf - Underhill, 1962 Alberta 8 38 33 2 Present study Alaska* Dixon, 1938 2 2t Rausch, 1961, 1970 * Q. collaris. 7 born. ~ based on scanty evidence. of the study. Animals on 10 discrete rock slides were live-trapped and individually marked. Certain females were retrapped and observed as often as possible through- out each breeding season. Young pikas emerging from nests beneath the rocks were associated with particular females, counted, and marked. The number of young associ- ating with a particular female was con- sidered to be the litter-size at weaning. Total populations were marked on 4 slides that were measured and mapped. Number of adults per unit area of rock slide provided estimates of population density. RESULTS Pikas in southwestern Alberta matured as yearlings (the spring followed their birth) and all females had the potential to produce two litters each breeding season. A comparison of breeding parameters among pikas throughout North America (Table 1) indicates that litter-size varies little and most populations (with the ex- ception of California) have two litters per year. Presumably, populations in areas with short summers do not have a suf- ficiently long period of favorable condi- tions to have animals maturing during the season of their birth (assuming growth rates similar to those in Alberta). A com- parison of breeding parameters among sev- eral species of Asian pikas (Table 2) indicates that different species have quite different breeding patterns, and that most Asian species have higher fecundity than pikas in North America. Mortality of Litters Entire litters were frequently lost prior to independence (48% of 67 females known to be pregnant failed to produce weaned young), but females that were successful had a constant pattern of fecundity. For example, potential litter size did not vary in relation to season, year, age and type of habitat. It is the steady erosion of poten- tial litter-size that is examined here. Mean litter-size was 2.64 at ovulation, 2.33 at birth, and 1.83 at weaning (Fig. 1). Thir- teen per cent of all ova shed were lost 216 136 J. S. MILLAR TasLe 2. Summary of reproductive parameters of Ochotonidae. Approximate Litters Mean Weight per embryo First Species (grams) Season Counts Breeding Source 1) O. alpina 130 J} Did Revin, 1968 2) O. alpina 2-3 3 yearling Khmelevskaya, 1961 3) O. alpina 2 2-37 yearling Yergenson, 1939% 4) O. alpina 115 1-2 2-6** Kistchinsky, 1969 5) O. daurica 2 iO summer of birth Nekypelov, 1954¢ 6) O. hyperborea 110 1 4.8 yearling Kapitonov, 1961 7) O. macrotis 180 2-3 5.0 yearling Zimina, 1962 8) O. macrotis 2-4 6.0 summer of birth Bernstein, 1964 9) O. pallasi 2-3 8.0 summer of birth Shubin, 19562 10) O. pallasi 5.8 summer of birth Chergenov, 1961% 11) O. pallasz 3 6.0 summer of birth Tarasov, 1950% 12) O. pusilla 200 3-5 9.0 summer of birth Shubin, 1965 13) O. rufescens 250 6.0 Puget, 1971 14) O. rutila 275 2-3 4.2 yearling Bernstein, 1964 15) O. princeps 135 2 223 yearling Present study 16) O. princeps 13 3-4 2.8 yearling Severaid, 1955 * mode. * range. Enot seen; cited by Bernstein, 1964. before birth while losses between birth ‘ ovulation and weaning were estimated at 21% (Millar, 1972b). The extent of losses in litters of different size was evaluated by comparing the frequencies of litter-sizes at conception, birth and weaning. Prenatal mortality al- most always involved only one embryo per litter, except when whole litters were lost. Assuming losses in all successful litters to involve only one offspring, an expected frequency was calculated by applying a a constant loss to each litter-size at the preceding stage. This expected frequency was then compared statistically («*) to the observed frequency. Prenatal, but not post- natal losses were compared directly in re- lation to initial litter size. -> Fic. 1. Frequencies of litter-size of pikas in southwestern Alberta at ovulation (based on counts of corpora lutea and corpora albicantia), birth (based on counts of healthy embryos after day 13 of gestation), and weaning (based on counts of young emerging from the rocks). weaning ND 4s 0) @ BRO 1S e@ Her cent We ee ae Zt litter- size 217 EVOLUTION OF LITTER-SIZE IN THE PIKA TABLE 3. 137 Mortality of embryos between conception and birth in relation to initzal litter-size at con- ception based on counts of corpora lutea and corpora albicantia. Observed litter-size at birth based on counts of healthy embryos in late gestation. Expected frequencies at birth based on a uniform 13% loss in all litters during gestation and assumes that only one embryo is lost from any one litter. . Observed Frequency at Conception . Percent Frequency at Conception . 13% loss [(13/100) & B] . Remaining (B-C) Gain From Next Largest Litter (C) Adjusted Frequency (D+ E) . Expected Frequency at Birth [(F/100) x 80] . Observed Frequency at Birth 2 x TODA OOD pp Litter-size 1 2 ) 4 Total ) 75 89 11 175 0 42.9 50.8 6.3 100 0 5.6 6.6 0.8 13 0) Sih28 44.2 5.5 87 5.6 6.6 0.8 0.0 13 5.6 43.9 45.0 55 100 4.5 S5ell 36.0 4.4 80 8 38 5) 1 80 2.7222 0.2396 0.2500 2.6272 5.8390; P > 1005; N:S. A comparison of frequency of litter-sizes between conception and birth (Table 3) indicated that the frequency of litters at birth was not significantly different from the frequency expected if mortality was equal among all litter-sizes. However, a direct comparison of prenatal losses in re- lation to potential litter-size (Table 4) indicated that although there were no dif- ferences between females ovulating two and three ova, those producing four ova suf- fered significantly greater losses than those shedding three. Potential litters of four were uncommon, and heavy losses resulted TABLE 4. Prenatal losses in successful pregnan- cies in relation to initial litter-sizes, based on differences between counts of corpora lutea and healthy embryos after day 13 of gestation (see Millar, 1972b). Tabulated as a percentage of fe- males that have losses and a percentage of ova that are lost. Sample sizes in parentheses. . Prenatal Losses Initial Litter-size % Females % Ova 2 212 13) 10.6 (66) 3 28.2 (39) 10:29 Ch 7)) 4 87.5* (8) Piel leot((6 72) * Significantly higher than in females shedding 3 ova (x°= 6.1871, P < .025). ** Significantly higher than in females shedding Srova (y= 5.28255 P< 1025). in almost no litters of four at birth. Similar differences in rates of mortality were ap- parent between birth and weaning. The frequency of litters at weaning was sig- nificantly different than expected if mor- tality was equal among all litter sizes at birth (Table 5). Litters of three were less common at weaning than expected, while litters of one and two were more common, indicating that greater mortality occurs in litters of three. Litters of three were com- mon at birth (41% of 80 litters contained three young), but rare at weaning (6% of 35 weaned litters contained three young) indicating that most females could raise only two young. Conceiving more offspring than can be raised may be advantageous in case an offspring is lost for some other reason. The fate of missing young is not known; only one dead nestling, estimated to be two weeks of age, was found. Index of Fat The sizes of particular fat bodies are difficult to relate to the condition of ani- mals because different fat bodies may be deposited or mobilized in response to changes in environmental (temperature, food supplies) conditions or physiological status (sex, age, breeding status) (Flux, 1971). The generalized fat index used here 218 138 TABLE 5. J. S. MILLAR Mortality of nestling pikas in relation to litter-size at birth. Observed litter-size at birth based on counts of healthy embryos in late gestation. Observed litter-size at weaning based on counts of young emerging from the rocks. Expected frequencies at weaning based on a uniform loss of 21% in all litters and assumes that only one nestling is lost from any one litter. Litter-size 1 2 3 4 Total A. Observed Frequency at Birth 8 38 33 1 80 B. Percent Frequency at Birth 10.0 47.5 41.2 13 100 C. 21% Loss [(21/100) x B)] Zeal 10.0 8.6 0.3 21 D. Remaining (B-C) 7.9 Sh is 32.6 1.0 79.0 E. Gain From Next Largest Litter (C) 10.0 8.6 0.3 0) 18.9 F. Adjusted Frequency (D+ E) 17.9 46.1 32.9 1.0 97.9 G. Adjusted Percent Frequency [(F/97.9) * 100] 18.3 47.1 33.6 1.0 100 H. Expected Frequency at Weaning [(G/100) x 35] 6.4 16.5 11.8 om 35 I. Observed Frequency at Weaning 8 25 2 (0) 35 x° 0.4000 4.3787 8.1389 0.3000 13.21 763 P < .005 (mg cardiac, splenic, interscapular fat per 100 gm body weight) presumably reflects general fat levels. Fat animals are not necessarily healthy animals, but fat animals must be obtaining, or at least storing, more energy in relation to their requirements than thin animals. In the pika, females enter the breeding season with much higher i — we w °o x< lu a = © 2 o ¢ 2 a re a z a WwW Ree fo) WW © 2 g¢ - & Bead. San ek ge ae nr aie S ° — Sy 2 Fic. 2. Mean index of fat (mg interscapular, cardiac and splenic fat per 100 gm body wt) of mature female pikas in southwestern Alberta in relation to stages of pregnancy and _ lactation. Vertical lines denote two standard errors each side of the mean. fat indexes than males, but lose these reserves over tne breeding season. A com- parison of fat reserves in relation to preg- nancy and lactation (Fig. 2) indicates that fat is deposited during pregnancy and drained during lactation. These drains occurred despite the presence of abundant food during the period of lactation, and did not vary in relation to littering period or type of habitat. Population Density This parameter is difficult to estimate, but pikas in southwestern Alberta exhibit several characteristics that indicate they are at or near saturation level. For instance, overall population levels were relatively stable over the three years of the study. Although individual popula- tions varied considerably (Table 6), yearly averages of adults per ha of rock were 7.5 in 1968, 5.8 in 1969 and 6.5 in 1970 (based on 0.8, 8.5 and 8.5 ha, respectively). Sec- ondly, pikas appeared relatively immune to variations in environmental conditions; no “catastrophes” were recorded. Thirdly, al- though few populations were dense enough to exhibit responses to density, low popu- lations produced more offspring per female to weaning than high populations, and any 219 EVOLUTION OF LITTER-SIZE IN THE PIKA 139 TABLE 6. Population parameters for five discrete populations of pikas in southwestern Alberta. Den- sity based on number of adult pikas per hectare of rock slide. Number of weaned young based on counts of young animals emerging from the rocks. Emigrants include only animals born in the popu- lations and whose final location was known. Transients and immigrants include all young animals caught on the area that were known not to be born there. No. Weaned No. Known Popu- No. Ad. No. Weaned Young per No. Known Transients and lations Density BS) Young Female Emigrants Immigrants il 4.0 5 9 1.80 3 1 2 4.1 14 eyo) - 1 3 5.4 6 14 PL eaXe; 3 i + 10.9 12 13 1.08 - - 5 22:0 6 2 0.33 - 1 populations that were still low after the lactation (Kaczmarski, 1966; Migula, breeding season could easily be replenished with immigrants (Table 6). These data indicate that the populations studied were probably at or near saturation level at all times. DISCUSSION Each female appears to be producing as many offspring as she can support. Females drain their energy reserves during lactation and large litters (three) appear to suffer higher mortality prior to independence than small litters (one and two). This limit of two offspring supported during lactation could be considered a local phe- nomena, but data from Colorado and Utah indicate that the same limit exists there. Counts of embryos from that area (Table 1) indicate that many females (16 of 26) gave birth to three or four young, while Krear (1965) noted that the number weaned was usually two. The limit imposed on litter-size during lactation did not appear related to environ- mental conditions since weather was rela- tively mild and food was abundant during the breeding season. The limit was more likely physiological; possibly based on one or more of three factors: energy assimila- tion, drainage of energy reserves, and the rate of growth of the young. Small mam- mals such as bank voles (Clethrionomys glareolus), common voles (Microtus ar- valis), mice (Mus musculus) and red squir- rels (Tamiasciurus hudsonicus) increase their food intake during pregnancy and 2 1968; Myrcha et al., 1969; Smith, 1968, respectively) and pikas likely do the same. Pikas also drain their reserves during lactation and apparently cannot support offspring through increased assimilation alone. Possibly, rather than draining their reserves below a critical level, or decreasing the size of each offspring, they sacrifice the size of the litter. The difference in energy expenditure between a female (mean weight 133 gm) supporting two and three offspring (weaning weight approximately 50 gm) would be considerable. Few studies were found where survival of young or condition of females was docu- mented for natural populations. Le Resche (1968) found greater mortality of twin moose calves (Alces alces) than single calves, and data collected by Markgren (1969) indicates a similar trend. ‘Tree mice (Phenacomys longicaudus) support only a certain biomass of offspring, even when fed an abundance of natural foods (Hamilton, 1962) and young rabbits (Oryctolagus cuniculus) in small litters grow faster than those in large litters (Myers and Poole, 1963), indicating that milk is limited. In general, the differential mortality in litters of different size during lactation ap- pear to be related to the female’s ability to support offspring. Prenatal mortality, how- ever, occurred early in gestation when em- bryos were very small in relation to the size of the female, and mortality at that time was not likely related to any nutritional stress on 0 140 the female. A possible explanation is that litter-size has been reduced over evolu- tionary time by limiting the capacity of the uterus, rather than by reducing the num- ber of ova shed. This could operate by limiting the number of embryos implanted, as in the elephant shrew (Elephantulus myurus) (Horst and Gillman, 1941) or through limiting the number of implanted embryos carried to term, as in the alpaca (Lama pecos) (¥Fernandex-Baca et al., 1970). Although most evolved reductions in litter-size undoubtedly arise through changes in ovulation rates, some sort of restriction placed on litter-size by the uterus may be relatively common. Greater prenatal losses in large litters have been noted in white-tailed deer (Odocoileus virginianus) (Ransom, 1967) and European rabbits (Oryctolagus cuniculus) (Poole, 1960), and the trend is evident in other data presented for European rabbits (Brambell, 1942; Lloyd, 1963; McIlwaine, 1962), European hares (Lepus europaeus) (Flux, 1967) and snowshoe hares (Lepus americanus) (Newson, 1964). Lack’s (1948) hypothesis that females produce as many offspring as they can sup- port appears to hold true for the pika. How- ever, his suggestion that the most frequent litter-size at birth is the most productive is not supported by my data, and has been criticized on theoretical grounds by Mount- ford (1968). Litters of three were common at birth, but were generally reduced to two young at weaning. Such a system may appear inefficient, but the ‘‘wastage” of one offspring would be selected against only if the wastage contributed in some way to the death of the parent or surviving off- spring. Perhaps, in pikas, there is an advantage in having an extra nestling available in case one is lost for some other reason before the critical period of lacta- tion. Spencer and Steinhoff (1968) suggested that animals with restricted breeding sea- sons have larger litters than those with extended breeding seasons to maximize the number of offspring produced during the J. S. MILLAR LITTER=SIZE LITTERS PER SEASON Fic. 3. Regression of mean litter-size against number of litters per breeding season of several species of pikas. Numbers refer to data in Table 2. A significant proportion of the variance of y is not explained by regression on x. (F = 1.4289, he > 25) females life span. From this, populations with short breeding seasons (hence fewer litters per year) should have the largest litters. A comparison of pika populations indicates no such trend (Fig. 3), while there is a trend (not significant) for large litters to be associated with long breeding seasons. Their assumption that maternal mortality varies directly with the size of the litter may be invalid (Tinkle, 1969). All behavioral or physiological attributes of a species can be related to the ability to survive or to reproduce. Since survival is a prerequisite to reproduction, it is likely that requirements for survival take priority over requirements for reproduction, and that females will sacrifice their litters be- fore threatening their own survival. In the pika, this is seen as a loss of total litters at high population densities and under other adverse conditions (Millar, 19720). The trend in litter-size among species may be attributed, at least in part, to body size. Species with large litters are generally larger than those with small litters (Table 2 Ne Lord (1960) predicted a positive cor- relation between litter-size and latitude in non-hibernating prey species. This is not true of the pika; litter-size is relatively constant in North America (Table 1). My data do not, however, refute his suggestion 221 EVOLUTION OF LITTER-SIZE IN THE PIKA Taste 7. Reproduction and adult mortality in populations of pikas. Adult Mortal- Litter- Litters/ Population ity size season Sources O. princeps 43.4 2.9 2 Present (Colorado study; John- and Utah) son, 1967; Hayward, 1952 O. princeps 46.0 2 Present study Alberta to ion) ) O. macrotis 53.2 6.0 2-4 Bernstein, 1964 O. rutila 64.8 4.2 2-3 Bernstein, 1964 * Based on per cent yearlings in mature popu- lations (see Millar and Zwickel, 1972a). that populations suffering low mortality produce relatively small litters because resources are limited. Mortality in Alberta was relatively low and litters were small (Table 7). The problem of determining the limited resource remains. Gibb (1968) considered food to be the important re- source, but pikas are herbivores that feed on a wide variety of plants, and food ap- peared abundant in Alberta. Cody (1966) suggested that successful offspring in saturated populations must be larger in order to be competitive. This may explain the partitioning of available ma- ternal resources into only two offspring (rather than three or four smaller off- spring). Perhaps the resource in question is space. Pikas are territorial (Kilham, 1958; Krear, 1965) and although detailed behavioral studies have not yet been done, competition for space likely occurs. SUMMARY Potential litter-sizes, mortality of em- bryos and nestlings, maternal fat reserves during pregnancy and lactation, and popu- lation parameters of pikas in southwestern Alberta are documented and used to evalu- ate several hypotheses on the significance of litter-size. Two, three, or sometimes four ova are shed at conception. Relatively 141 heavy losses in litters of four occur during gestation. These losses are not likely caused by any nutritonal stress on females, and may be related to an evolutionary re- duction in litter-size by limiting the capac- ity of the uterus. Relatively heavy losses in litters of three between birth and wean- ing, and low maternal fat reserves during lactation indicate that females produce as many offspring as they can support. Popu- lation appeared at or near saturation level, and the advantage in partitioning maternal resources into two, rather than three or four smaller offspring may be that the better nourished offspring are more successful at competing for space. ACKNOWLEDGMENTS This study was conducted under the supervision of Dr. F. C. Zwickel and was supported by funds from the National Re- search Council of Canada and the De- partment of Zoology and the R. B. Miller Biological Station, University of Alberta. R. A. MacArthur and H. Reynolds pro- vided assistance during 1969 and 1970, respectively. Special thanks are due to F. C. Zwickel, J. O. Murie, S. C. Tapper, J. P. Ryder, A. E. Aubin and C. D. Ankney, for many valuable comments, suggestions, criticisms and heated arguments. LITERATURE CITED ANDERSON, S. 1959. Mammals of the Grand Mesa, Colorado. Univ. Kansas Publs. Mus. Nat. Hist. 9:405-414. Battey, V. 1936. The mammals and life zones of Oregon. North Amer. Fauna No. 55:112- 117. Bernstein, A. D. 1964. The reproduction by red pika (Ochotona rutila Sev.) in the Zailijsk Alutau (In Russian). Bull. Mosc. Soc. Nat., Biol. 69:40-48. BraMBeELL, F. W. R. 1942. Intra-uterine mor- tality of the wild rabbit. Oryctolagus cunic- ulus (L.). Proc. Roy. Soc. B. 130:462-479. Copy, M. L. 1966. A general theory of clutch size. Evolution 20:174-184. Dice, L. R. 1926. Pacific coast rabbits and pikas. Occ. Papers Mus. Zool., Univ. Mich. 166:1-28. ——. 1927. The Colorado pika in captivity. J. Mammal. 8:228-231. Dixon, J. S. 1938. Birds and Mammals of 222 a. rn _ ho Mount McKinley National Park, Alaska. Nat. Park Service, Fauna Ser. 3, 236 p. FERNANDEZ-Baca, S., W. HANSEL, AND C. Novoa. 1970. Embryonic mortality in the alpaca. Biol. Reprod. 3:243-251. Frux, J. E. C. 1967. Reproduction and body weights of the hare, Lepus europaeus Pallas, in New Zealand. N.Z.J. Sci. 10:357-401. 1971. Validity of the kidney fat index for estimating the condition of hares: a dis- cussion. N.Z.J. Sci. 14:238-244. Giss, J. A. 1968. The evolution of reproductive rates: are there no rules? Proc. N.Z. Ecol. Soc. 15:1-6. GRINNEL, J., J. Dixon, anD J. M. Linspace. 1930. Vertebrate natural history of a section of northern California through the Lassen Peak region. Univ. Cal. Publ. Zool. 35:1-594. Hatt, E. R. 1946. Mammals of Nevada. Univ. Calif. Press. 710 p. Hamitton, W. J. 1962. Reproductive adapta- tions in the red tree mouse. J. Mammal. 43:486-504. Haywarp, C. L. 1952. Alpine biotic communities of the Uinta Mountains, Utah. Ecol. Monogr. 22:93-102. Horst, C. J. V. D., anp J. Grrrman. 1941. The number of eggs and surviving embryos in Elephantulus. Anat. Rec. 80:443-452. Jounson, D. R. 1967. Diet and reproduction of Colorado pikas. J. Mammal. 48:311-315. KaczMarskI, F. 1966. Bioenergetics of preg- nancy and lactation in the bank vole. Acta Theriol. 11:409-417. Kapironov, V. I. 1961. Ecological observations on Ochotona hyperborea Pall. in the lower part of the Lena River. (In Russian; English summary). Zool. Zh. 40:922-933. KHMELEVSKAYA, N. V. 1961. On the biology of Ochotona alpina Pallas. (In Russian; English summary). Zool. Zh. 40:1583-1585. Kirwam, L. 1958. Territorial behavior in pikas. J. Mammal. 39:307. Kistscutnsky, A. A. 1969. The pika (Ochotona alpina hyperborea Pall.) in the Kolyma high- lands. (In Russian; English summary). Bull. Mosc. Soc. Nat. Biol. 74:134-143. Krear, H. R. 1965. An ecological and ethologi- cal study of the pika (Ochotona princeps saxi- tilis Bangs) in the Front range of Colorado. Ph.D. Thesis, Univ. of Colorado, Boulder. 329 p. Lack, D. 1948. The significance of litter-size. J. Anim. Ecol. 17:45-50. Le Rescue, R. E. 1968. Spring-fall calf mor- tality in an Alaska moose population. J. Wild- life Manage. 32:953-956. Luioyp, H. G. 1963. Intra-uterine mortality in the wild rabbit, Oryctolagus cuniculus (L.) in populations of low density. J. Anim. Ecol. 32:549-563. 223 J. S. MILLAR Lonc, W. S. 1940. Life histories of some Utah mammals. J. Mammal. 21:170-180. Lorp, R. D. 1960. Litter-size and latitude in North American mammals. Am. Midl. Nat. 64:488-499, Markcren, G. 1969. Reproduction of moose in Sweden. Viltrevy 6:127-299. McIztwainer, C. P. 1962. Reproduction and body weights of the wild rabbit Oryctolagus cuniculus (L.) in Hawke’s Bay, New Zealand. N-Z.J). sci. 52324-3411. Micura, P. 1969. Bioenergetics of pregnancy and lactation in the European common vole. Acta Theriol. 14:167-179. Miirar, J. S. 1972a. Timing of breeding of pikas in southwestern Alberta. Can. J. Zool. 50:665-669. Success of reproduction in pikas (Ochotona princeps Richardson) Fecudity of pikas in relation to the environment. (in preparation). Murar, J. S., ano F. C. ZwickeL. 1972a. De- termination of age, age structure, and mor- tality of the pika, Ochotona princeps (Rich- ardson). Can. J. Zool. 50:229-232. , AND Characteristics and ecological significance of hay piles of pikas. Mammalia (in press). Mountrorp, M. D. 1968. The significance of litter-size. J. Anim. Ecol. 37:363-367. Myers, K., anp W. E. Poore. 1963. A study of the wild rabbit Oryctolagus cuniculus (L.) in confined populations. V. Population dy- namics. C.S.I.R.O. Wildlife Research. 8:166- 203. Myrcua, A., L. RyszkowskI, AND W. WALKowWA. 1969. Bioenergetics of pregnancy and lactation in white mouse. Acta. Theriol. 14:161-166. Newson, J. 1964. Reproduction and prenatal mortality of snowshoe hares on Manitoulin Island, Ontario. Can. J. Zool. 42:987-1005. Pootr, W. E. 1960. Breeding of the wild rabbit, Oryctolagus cuniculus (L.) in relation to the environment. C.S.I.R.O. Wildlife Research 5: 21-43. Pucet, A. 1971. Ochotona r. rufescens (Gray 1842) in Afghanistan and its breeding in cap- tivity. (In French; English summary). Mam- malia 35:24-37. Ransom, A. B. 1967. white-tailed deer in Manage. 31:114-123. Rauscu, R. L. 1961. Notes on the collared pika, Ochotona collaris (Nelson), in Alaska. Mur- relet. 42:22-24. Reproductive biology of Manitoba. J. Wildl. 1970. Personal communication, College, Alaska. Revin, Y. N. 1968. A contribution to the biology of the northern pika (Ochotona alpina Pall.) on the Olekmo-Charskoe highlands (Yukatia). (In Russian; English summary). Zool. Zh. 47:1075-1082. EVOLUTION OF LITTER-SIZE IN THE PIKA Rorest, R. I. 1953. Notes on pikas from the Oregon Cascades. J. Mammal. 34:132-133. SEVERAID, J. H. 1955. The natural history of the pika (Mammalian genus Ochotona). Ph.D. Thesis, Univ. of Calif. 820 p. Suusin, I. G. 1965. Reproduction of Ochotona pusilla Pall. (In Russian; English summary). Zool. Zh. 44:917-924. Spencer, A. W., AND H. W. STEINHOFF. 1968. An explanation of geographical variation in litter-size. J. Mammal. 49:281-286. SmitH, C. C. 1968. The adaptive nature of social organization in the genus of three squir- rels Tamiasciurus. Ecol. Monographs 38:31-63. SmitH, M. H., anp J. T. McGinnis. 1968. 143 Relationships of latitude, altitude, and body size to litter size and mean annual production of offspring in Peromyscus. Res. Popul. Ecol. X:115-126. TinkLe, D. W. 1969. The concept of reproduc- tive effort and its relation to the evolution of life histories of lizards. Amer. Natur. 103: 501-516. UNpDERHILL, J. E. 1962. Notes on pika in cap- tivity. Can. Field Nat. 76:177-178. ZIMINA, R. P. 1962. The ecology of Ochotona macrotis Gunther dwelling in the area of the Tersky-Alutau mountain range. (In Russian; English summary). Bull. Mosc. Soc. Nat., Biol. 67:5-12. 224 Sonderdruck aus Z. f. Saugetierkunde Bd. 30 (1965), H. 1, S. 10—20 Alle Rechte, auch die der Ubersetzung, des Nachdrucks und der photomechanischen Wiedergabe, vorbehalten. VERLAG PAUL PAREY - HAMBURG1 _: SPITALERSTRASSE 12 The effects of suckling on normal and delayed cycles of reproduction in the Red Kangaroo By G. B. SHARMAN Eingang des Ms. 23. 12. 1963 Introduction In non-lactating female marsupials the occurrence of fertilization, followed by imme- diate gestation of the embryo, does not delay the onset of the following oestrus. In those marsupials in which the gestation period is considerably shorter than the length of one oestrous cycle, such as Didelphis virginiana (HaRTMAN, 1923) and Trichosurus vulpecula (PILTON and SHARMAN, 1962), oestrus recurs at the expected time if the young are removed at birth. In several species of Macropodidae, such as Setonix brachyurus (SHARMAN, 1955), Potorous tridactylus (HuGuEs, 1962) and the Red Kangaroo (SHaR- MAN and Catasy, 1964), the gestation period occupies almost the length of one oestrous cycle and oestrus is imminent at the time of parturition. Oestrus thus recurs just after the young reach the pouch (post-partum oestrus) presumably because pro-oestrus chan- ges are initiated before the onset of the suckling stimulus. In all marsupials suckling of young in the pouch is accompanied by a lengthy period during which oestrus does not occur. This period is called the quiescent phase of lactation or, simply, the quies- cent phase. It differs from seasonal anoestrus in that the ovaries and other reproduc- tive organs respond to the removal of the suckling stimulus by resuming cyclic func- tions. Those marsupials in which post-partum oestrus occurs exhibit discontinuous embryonic development analogous to the delayed implantation which occurs in some eutherian mammals. If fertilization takes place at post-partum oestrus the resulting embryo assumes a dormant phase, at the blastocyst stage, and is retained as a dormant blastocyst during the quiescent phase. In these marsupials pregnancy (the interval between copulation at post-partum oestrus and parturition) is long and gestation of the embryo is interrupted by the dormant phase. In the Red Kangaroo, Megaleia rufa (Desm.), the oestrous cycle averages 34 to 35 days and the gestation period is 33 days in length (SHARMAN and Carasy, 1964). Post- partum oestrus occurs, usually less than 2 days after the newborn young reaches the pouch, and a dormant blastocyst is found in the uterus of females, fertilized at post- partum oestrus, which are suckling young less than 200 days old in the pouch (SHAR- MAN, 1963). If the young is removed from the pouch suckling ceases and the dormant blastocyst resumes development: the young derived from it being born about 32 days after removal of the pouch young (RPY). This birth is followed by another post- partum oestrus or, if the female was not carrying a blastocyst, by a normal oestrus. Oestrus recurs at the same number of days after RPY irrespective of whether a de- layed blastocyst was carried or not. The sequence of events from RPY to the next oestrus is called the delayed cycle of reproduction! to distinguish it from the normal reproductive cycle which follows oestrus. The delayed reproductive cycle may be divided into delayed gestation and delayed oestrus cycle according to whether a dor- 1 The term "delayed cycle of reproduction“ or ”delayed (reproductive) cycle“, was introduced by TynpaLe-Biscor (1963) to describe the resumption of ovarian activity, and the features associated with it, following removal of pouch young (RPY). bo bo Ol Normal and delayed cycles of reproduction in the Red Kangaroo ula mant blastocyst does or does not complete development. If the young is retained in the pouch until it leaves in the normal course of events the delayed reproductive cycle occurs coincident with the latter stages of pouch life. The dormant phase of the blastocyst gives way to renewed development when the pouch young is a little over 200 days old and subsequent vacation of the pouch, at an average age of 235 days, is immediately followed by birth of another young (SHARMAN and Caraby, 1964). The young is suckled for another 130 days, that is until it is about a year old, after it leaves the pouch. During this period the normal reproductive cycle occurs if the pouch is not occupied. It is thus evident that, although the delayed reproductive cycle occurs after RPY and cessation af lactation, some factor other than the actual pro- duction of milk must be implicated for both delayed and normal cycles may also occur during lactation. The aim of the experiments reported below was to determine the effect of the suckling stimulus on both normal and delayed reproductive cycles. Additional suck- ling stimulus was provided by fostering an extra young on to females already suck- ling a young-at-foot. The experimental approach was suggested by chance obser- vations on a female Red Kangaroo which, while suckling her own young-at-foot, alternately fed the young of another female kept in the same enclosure. There are four teats in the pouch but the teat to which the young attaches after birth alone produces milk and its underlying mammary gland produces all the milk for the young from birth to weaning. The female’s own young and the foster-young thus shared the products of a single mammary gland and used the same teat alternately. Some initial results, in so far as they were relevant to the theme of delayed implanta- tion, were reported earlier in a review of that subject (SHARMAN, 1963). Methods The results presented consist of observations on a minimum of five reproductive cyc- les in the female Red Kangaroo in each of the following categories: . Normal cycle of reproduction, suckling one young-at-foot. Normal cycle of reproduction, suckling two young-at-foot. Delayed cycle of reproduction, suckling one young-at-foot. Delayed cycle of reproduction, suckling two young-at-foot. RW NY eS The results are compared with data on the normal and delayed cycles of reproduc- tion in non-lactating females most of which have been published elsewhere (SHARMAN, 1963; SHARMAN and Catrasy, 1964; SHARMAN and PiLtTon, 1964). In most cases the experimental females were pregnant or carrying dormant blastocysts so that cycles of normal or delayed gestation with subsequent post-partum oestrus were studied. The gestation periods and cycles were regarded as having been significantly lengthened when they occupied a time greater by the length of two, or more, standard deviations than similar cycles in control, non-lactating, females Some difficulty was experienced in getting females to accept foster-young and only six females readily did so. The experiments were therefore done serially one female being used in two and two females in three experiments. The animals were watched from a hide overlooking the enclosures and observed with binoculars. An initial watch was always done to find whether females accepted their potential foster-young. Thereafter prolonged watches were kept on some females to determine the amount of time spent suckling the young-at-foot. Vaginal smears for the detection of oestrus and copulation were taken as reported previously (SHARMAN and Catasy, 1964). 226 12 G. B. Sharman Results Effects of suckling on the normal cycle of reproduction In thirteen non-lactating female Red Kangaroos forty-two intervals from oestrus to the succeeding oestrus averaged 34.64 days with a standard deviation of 2.22 days (34.64 + 2.22 days). Twenty gestation periods in fourteen females lasted 33.00 + 0.32 days (Fig. 1A). In five females, each observed for a single reproductive cycle while suckling one young-at-foot, the intervals between two successive oestrous periods were not different from those in non-lactating females (Fig. 1B). In another female (K32a) A 42cycles a) K60 B Cc 0 4 8 12 16. ~ 20 24 728 932636 40 = =44 48 Intervals between successive oestrous periods Fig. 1. Intervals between successive oestrous periods in nonlactating (control) female Red Kangaroos (A), females suckling one young-at-foot (B) and females suckling two young-at- foot (C). Black lines — continuous embryonic development, broken lines — approximate eriods of dormant phase in embryo induced and maintained by suckling young-at-foot, open ee — no embryos present, bars inserted in A — standard deviations either side of mean. the gestation period was not significantly different from that of control females but oestrus did not occur until 5 days post-partum. This was the longest interval between parturition and post-partum oestrus recorded but it is not regarded as significant. Two cycles in female K31, one lasting 41 days and one 47 days, were abnormally long. The 41-day cycle is of special significance since the interval between copulation and birth was 40 days. This differs so much from the gestation period in the control, non-lacta- ting, females that it must be assumed that suckling of the single young-at-foot induced a short quiescent phase in the uterus accompanied by a dormant phase of about 7 days in the embryo. The 47-day cycle was over 12 days longer than the mean normal cycle length and 7 days longer than the maximum cycle length. The female copulated at oestrus but did not give birth so it is presumed that fertilization did not occur. In three females already suckling one young-at-foot, which had another young-at- foot fostered on to them at about the time of fertilization, the lengths of the repro- ductive cycles were not significantly different from those in control females. Two females had significantly longer cycles than in control females. One of these (K36) was used in three successive experiments while suckling the same two young-at-foot. In the first of these (K36a) the extra suckling stimulus had no significant effect on the length of the reproductive cycle. The second experiment concerned the delayed reproductive cycle and is reported below. During the third experiment (K36c) the young were being weaned but a highly significant result was obtained. The interval from copulation to 227 yp) Normal and delayed cycles of reproduction in the Red Kangaroo 13 birth showed conclusively that a dormant phase had been induced and maintained in the embryo for about 14 days of the 47-day pregnancy. In the other female in which the cycle was prolonged (K4e) the embryo presumably had a dormant phase of about 6 days. Effects of suckling on the delayed cycle of reproduction In ten non-lactating females thirteen intervals from RPY to the succeeding oestrus were 34.46 + 1.92 days. In seven of these females the delayed gestation period was 31.64 + 0.65 days (Fig. 2A). There was no evidence that suckling one young-at-foot had any effect on the length of the delayed reproductive cycle (Fig. 2B). In one female (K12a) the interval from RPY to the following oestrus was 38 days but this falls short of the minimum interval accepted as significantly different. All six females suckling two young-at-foot (Fig. 2C) were carrying a dormant blastocyst in the uterus when the pouch young were removed. In five of these the interval RPY to birth was significantly longer than in control females (Fig. 2C). The interval RPY to the next oestrus was longer than the mean for control non-lactating females in all six experimental females and in three of them (K4b, K30b, K36b) the difference from controls was highly significant. It must be concluded that the blasto- cysts of five of the above experimental females remained in the dormant phase for between 3 and 22 days longer after RPY than did those of control non-lactating females and females suckling one young-at-foot. 13 cycles K 4a K15 K38b K12b K12a K38a K63b K32b K36b K 30b Intervals between RPY and oestrus Fig. 2. Intervals between removal of pouch young (RPY) and the next oestrus in non-lactating (control) female Red Kangaroos (A), females suckling one young-at-foot (B) and females suckling two young-at-foot (C). Black lines — continuous embryonic development, broken lines — approximate periods of continued dormant phase of embryo maintained by suckling young-at-foot, bars inserted in A — standard deviations either side of mean. The amount suckling in relation to occurrence of parturition and return to oestrus Observations on the habits of the pouch young suggested that the stimulus causing withholding of the mother’s reproductive cycles might be tactile and received via the teat. The young during the early stages of pouch life, when reproductive cycles were withheld, were suckled continuously and could not regain the teat if removed before the age of 6 weeks. Later young were able to take the teat back into their mouths but were seldom found free of the teat before the age of about 5 months. On the other 228 14 Table 1 Effects of suckling one and two young-at-foot on subsequent parturition and oestrus in Red Kangaroos Effects of suckling on subsequent Minutes of suckling Ages of joung (days) parturition and oestrus on a] } ec — 3 6 Zz ae} uv ie & a2 IS) we ° So a 2 i ae) wa boo ane) 3) i) e) Occurrence of parturition Per day oo G 3 ) a 4 v 3 ) isa oD S =] 8 BS cq z e) Own young Foster-young when expected late when expected late normal normal 78 44 1355 1555 96 259 255 48 31 203 late no young born normal 51 269 288 when expected when expected normal 68 38 1385 G. B. Sharman 53 316 138,5 All females suckling 1 young late late normal delayed 150 55 31 86 27 192 259 2255 309 B22 when expected late late 90 85 1535 78 late delayed 83 98 169 305 116 All females suckling 2 young hand the pouch young present when the delayed reproductive cycle occur- red apparently frequently released the teat as they were seen protruding their heads from the pouch to feed from the ground or leaving the pouch entirely (SHARMAN and Catasy, 1964). Theoretically it was to be expected that if repro- ductive cycles resumed in response to a_ lowered suckling stimulus, as they did during the terminal stages of pouch feeding, then the cycles which occurred as soon as the young left the pouch should have been of nor- mal length. Six of the eight cycles shown in Fig. 1B were the first which oc- curred after termination of pouch feeding. Four were of normal length but two cycles in one female (K 31a,b) were lengthe- ned by a_- significant amount. Observations on the habits of the young, just after they left the pouch permanently, showed that they frequently attempted to regain the pouch but were restrained from doing so by their mothers (SHARMAN and Catapsy, 1964). In these cases they spent long periods with their heads in the pouch during which time they may have grasped the teat. It is also possible that the young, subjected permanently for the first time to the cooler environ- ment outside the pouch, fed more frequently than they did during the ter- Normal and delayed cycles of reproduction in the Red Kangaroo 15 minal stages of pouch life. This would result in a greater suckling stimulus being exerted: at least during the initial stages of life outside the pouch. A number of females suckling one or two young-at-foot were watched continuously for varying periods and the amounts of time spent suckling were recorded (Table 1). It was at once apparent that females feeding two young-at-foot spent nearly twice as much time suckling as did females with a single young-at-foot. The relationship bet- ween amount of suckling and interruption or resumption of the reproductive cycle is, however, not so obvious. Thus, in female K31, 48 and 51 minutes of suckling per day were associated with lengthening of the interval between successive oestrous periods and 48 minutes per day with inducing and maintaining a short dormant phase in the embryo. In two other females (K60, K30c) a greater amount of suckling apparently had no effect on the length of the cycle or on pregnancy. However, although the watches were done during the relevant cycles, they were not necessarily done at the critical period of the cycle when the suckling stimulus exerted its effect. This period could not be ascertained since no evidence of its occurrence was available until the females gave birth or returned to oestrus. The figures in Table 1 are thus to be regar- ded as no more than a guide to the amount of suckling which occurred at the critical period. The most conclusive evidence about the effect of the suckling stimulus on the re- productive cycle came from the females from which pouch young were removed while they were suckling two young-at-foot (Fig. 2C). In one of these females (K38a) the suckling of two young-at-foot was without effect on the delayed reproductive cycle; in three (K32b, K36b, K63b) the delayed cycle began while two young were being suckled but in two others (K4b, K30b) the delayed cycle was only initiated when one of the suckling young-at-foot was removed. The interval from removal of the young-at-foot to completion of the delayed cycle was approximately the same (31—32 days) as from RPY to the completion of the cycle in the control females. The two intervals between successive oestrous periods with intervening pregnan- cies which were observed in the same female (K36a, c) while suckling the same two young-at-foot call for some comment. Parturition and return to oestrus occurred when expected in the first cycle but were delayed significantly in a subsequent cycle when the young were much older and were being weaned (Fig. 1C). During this, latter, cycle one of the young frequently grasped the teat for periods of 10 minutes or more but when the female’s pouch was examined it was found that no milk could be expressed from the teat and that the mammary gland was regressing. This was in contrast to the condition in other females suckling young-at-foot in which milk could usually be readily expressed. No watch was done to observe the amount of time the young spent sucking the dry teat as the significance of the observation was only realised after completion of the cycle. This cycle is, however, of particular significance because it appears likely that the suckling stimulus, in the absence of lactation, in- duced a quiescent phase in the uterus lasting some 14 days and a corresponding period of dormancy in the blastocyst. Discussion Delayed implantation in the Red Kangaroo is of the type usually referred to as lacta- tion controlled delayed implantation. This description is adequate in so far as the delayed cycle of reproduction is initiated following removal of the pouch young and cessation of lactation. However, the delayed cycle also occurs during the seventh and eighth months of the 12-month lactation period. It therefore follows that, in these cases, the delayed cycle does not begin in response to the cessation of lactation or to the imminent cessation of lactation. The quiescent phase of lactation with asso- 230 16 G. B. Sharman ciated arrested development of the embryo is initiated during the early part of lac- tation while a small young is suckled continuously in the pouch but the normal re- productive cycle may, as has been shown above, occur during the latter part of lac- tation. It is thus much more likely that the amount of suckling stimulus which the female receives at various phases of the lactation period is of paramount importance in determining whether the normal reproductive cycle shall be interrupted or whether the delayed cycle shall be initiated. The experiments reported above have shown that in some females the normal cycle is interrupted and a quiescent phase of lactation, with associated dormant phase of the embryo is induced by increasing the suckling stimulus. It has also been shown that the stimulus of suckling of young, outside the pouch, is capable of prolonging the quiescent phase of lactation and dormant phase of the embryo. Two other factors could be of importance in determining the time of onset of the delayed cycle of reproduction: 1. Temporary or permanent vacation of the pouch. 2. Fall in milk yield. Temporary emergence from the pouch first occurs when the young are less than 190 days old and permanent emergence at the average age of 235 days — that is a few days before the completion of the delayed cycle (SHARMAN and Carasy, 1964) but the delayed cycle apparently begins when the young are a little over 200 days old. Precise data on this point are difficult to obtain but assu- ming that the delayed cycle, once initiated, proceeds at the same rate in lactating females as it does in females from which the pouch young are removed then it must begin about 30 days before the young leaves the pouch. This is in agreement with the massive amount of data obtained from Red Kangaroos taken in the field. The onset of the delayed cycle can hardly occur in response to a fall in milk yield since it takes place when the young is actively growing and when it is increasing rapidly in weight. From the age of 200 days to the age of 220 days, during which period the delayed cycle is resumed, the pouch young increase from about 2.5 to 3.5 kg in weight which is not the expected result of a fall in milk yield. Furthermore removal of young from the pouches of females which were suckling two young-at-foot must have been ac- companied by a fall in milk yield yet under these circumstances the quiescent phase of lactation with associated dormant blastocyst continued in five of six females (Higss2@). The importance of the suckling stimulus in marsupial reproduction was demon- strated by SHARMAN (1962) and SHARMAN and Catasy (1964) who transferred new- born young Trichosurus vulpecula and Megaleia rufa to the pouches or teats of non- lactating, non-mated or virgin females of each of these species at the appropriate number of days after oestrus. The suckling stimulus exerted by the young induced the onset of lactation without the prior occurrence of pregnancy and oestrous cycles were withheld while the foster-young were suckled in the pouch. SHARMAN and Ca- LABY (1964) were unable to demonstrate any behavioural differences between preg- nant and non-mated female Red Kangaroos at the same number of days after oestrus except that pregnant females repeatedly cleaned their pouches just before giving birth. Other authors (Hit and O’Donocuug, 1913; Hartman, 1923; SHARMAN, 1955; Pit- TON and SHARMAN, 1962) have drawn attention to the remarkable resemblances of post-oestrous changes in pregnant females to those of non-mated females in various species of marsupials. It is apparent, that whereas in polyoestrous eutherian mammals hormones produced by the embryonic membranes modify the reproductive cycle and prevent the recurrence of oestrus during pregnancy, no such mechanism has yet been demonstrated in any marsupial. In those marsupials which do not have a seasonal anoestrous period, such as the Red Kangaroo, the reproductive cycle is continuous except when interrupted by the quiescent phase of lactation. Owen (1839-47) determined the gestation period (interval from mating to birth) 231 Normal and delayed cycles of reproduction in the Red Kangaroo 17 of a lactating female Great Grey Kangaroo as 38—39 days. HrEpiGER (1958) stated that K. H. WinkELsTRATER and E. CrisTEN in Zurich Zoo found gestation periods of 30 and 46 days in the same species and later, in the same paper, stated that a young was born on the forty-sixth day after mating in a lactating female Great Grey Kangaroo. However the dates quoted by HepicEr show that the gestation period“ was actually 57 days. In non-lactating Great Grey Kangaroos Miss PHyLiis PILTON (pers. comm.) found the gestation period was about 30 days and in the C.S.I.R.O. Division of Wildlife Research four gestation periods in three non-lactating females were 33 days 6 hours to 34 days 6 hours, 33 days 18 hours to 34 days 10 hours, 34 days to 34 days 17 hours and 34 days to 34 days 20 hours. It is apparent that, although the Great Grey Kangaroo does not have the same type of lactation con- trolled delayed implantation as occurs in the Red Kangaroo and other marsupials (SHARMAN, 1963), intervals between mating and birth in lactating females may be an unreliable guide to the gestation period. HEpIGER (1958) stated that exact gestation periods in kangaroos and other marsupials are difficult to determine because ovulation occurs several days after mating and spermatozoa can remain active in the oviduct for long periods. This may be true of the marsupial Dasyurus viverrinus, but Hitt and O’DonocuHue’s (1913) work on this species has not been repeated and confirmed. Delayed ovulation and storage of spermatozoa do not occur in Didelphis (HARTMAN, 1923), Setonix (SHARMAN, 1955) or Trichosurus (PILTON and SHARMAN, 1962) and gestation periods in non-lactating females of these species can be determined with considerable accuracy. In the Red Kangaroo the intervals between mating and birth in some lactating females (Table 2) are not true gestation periods since they include Table 2 Intervals from mating to birth and intervals from removal of pouch young (RPY) to birth in seven female Red Kangaroos subjected to different levels of suckling stimulus No. of female K c < K 36 Intervals from mating to birth Non-suckling — 33 as Suckling 1 young = Suckling 2 young — 32,47 Intervals from RPY to birth Non-suckling Suckling 1 young Suckling 2 young a period of arrested development of the embryo. However, in thirteen non-lactating female Red Kangaroos one gestation period was 32 days, one was 34 days and eighteen were 33 days in length (SHARMAN and Catasy, 1964). The true gestation period, as in the species above, can therefore be determined with precision. Perhaps failure to recognise the importance of the suckling stimulus accounts for the inaccuracy of some of the marsupial gestation periods given in International Zoo Year Book Vol. 1 (Jarvis and Morris, 1959). The list is incomplete and at least half of the figures given are wrong. 232 18 G. B. Sharman The occurrence of lactation controlled delayed implantation in marsupials was re- ported in 1954 (SHARMAN, 1954) and numerous papers have since appeared indicating that it is of widespread occurrence among kangaroo-like marsupials. Records of birth in captive female marsupials after long isolation from males, such as those reported by Carson (1912) in the Red Kangaroo and, recently, by HepicEer (1958) in Bennett’s Wallaby, are readily explained in terms of the occurrence of delayed implantation. I am indebted to Miss Pat Bercer, Mr. JOHN Lipke and Mr. James MERCHANT who helped with animal maintenance, handling and watching. The interest, assistance and advice on the manuscript given by my colleague Mr. J. H. Caray is gratefully acknowledged. Summary In non-lactating female Red Kangaroos the oestrous cycle lasted about 35 days and the gestation period was about 33 days. Gestation did not interrupt the oestrous cycle. Postpartum oestrus, at which copulation and fertilization took place if the female was with a male, occurred just after parturition. Recurring reproductive cycles were replaced by the quiescent poate of lactation for up to about 200 days while the young were suckled in the pouch. If ertilization occurred at postpartum oestrus a dormant blastocyst was carried in the uterus during the quiescent phase of lactation. The delayed cycle of reproduction during which the hitherto dormant blastocyst, if present, completed development occurred following removal of young less than 200 days old from the pouch. If the young were retained in the pouch until they emerged in the normal course of events the delayed cycle of reproduction occurred coincident with the last month of pouch life and was completed a day or two after the young permanently left the pouch. Suckling of the young occupied one year: they were suckled for about 235 days in the pouch and for a further 130 days after leaving the pouch. The delayed cycle of reproduction could thus occur during, and long before the cessation of, lactation. Normal cycles of reproduction occurred during lactation if the pouch was not occupied. The lengths of normal and delayed cycles of reproduction in females suckling one and two i a ta were compared with those in control, non-lactating, females. The results were as follows: Normal cycle of reproduction Females suckling one young-at-foot. Six cycles not significantly different from those of controls; two cycles significantly longer than in controls in one of which a dormant phase of about 7 days occurred in the embryo. Total: 8 cycles. Females suckling two young-at-foot. Three cycles not significantly different from those of control females: two cycles significantly longer than in control females which included dor- mant periods of 6 and 14 days in the embryos. Total: 5 cycles. Delayed cycle of reproduction Females suckling one young-at-foot. No effect of suckling. Total: 5 cycles. Females suckling two young-at-foot. One cycle not significantly different from those of control females. Five cycles longer than those of control females in which the dormant periods of the blastocysts were extended by 3, 3, 6, 11 and 22 days. In the two latter cycles resumption of development of the dormant blastocysts did not occur until removal of one of the suckling young-at-foot. Total: 6 cycles. Observations showed that females with two young-at-foot suckled their young for about twice the length of time that females suckled a single young-at-foot. It was concluded that the suckling stimulus exerted by one or two young-at-foot could induce and maintain the quiescent phase of lactation and the associated dormant phase in the embryo. Available evidence suggested that the stimulus causing onset of the quiescent phase was tactile and received via the teat and that the delayed cycle of reproduction occurred, or the interrupted normal cycle was resumed, when the suckling stimulus was lessened. It is suggested that some published gestation periods of marsupials owe their error to the failure of observers to appreciate the significance of concurrent suckling. Reported cases of female marsupials giving birth after long isolation from males can readily be explained as due to the occurrence of the delayed cycle of reproduction. 233 Normal and delayed cycles of reproduction in the Red Kangaroo 19 Zusammenfassung Bei nichtsdugenden QQ des Roten Riesenkanguruhs dauert der Oestrus-Cyclus rund 35 Tage, die Trachtigkeit rund 33 Tage. Trachtigkeit unterbricht den Cyclus nicht. Postpartum- Oestrus, bei dem Begattung und Befruchtung stattfanden, erfolgten unmittelbar nach der Geburt. Wiederkehr des Oestrus wurde durch eine Latenz wahrend der Laktation bis zu 200 Tagen verhindert, wahrend welcher das Junge im Beutel gesdugt wurde. Wenn beim Postpar- tum-Oestrus Befruchtung erfolgt war, enthalt der Uterus wahrend dieser Latenzperiode eine ruhende Blastocyste. Der verzOgerte Cyclus der Fortpflanzung, wahrend der die bisher ruhende Blastocyste (wenn sie vorhanden ist) ihre Entwicklung vollendet, tritt auf, wenn das Junge friiher als 200 Tage nach der Geburt aus dem Beutel entfernt wird. Wenn die Jungen jedoch so lange im Beutel bleiben, bis sie ihn normalerweise verlassen hatten, fallt der verzogerte Cyclus der Fortpflanzung mit dem letzten Monat des Beutellebens zusammen und ist vollendet ein oder zwei Tage nachdem die Jungen den Beutel endgiiltig verlassen haben. Das Saugen dauert ein volles Jahr: die Jungen werden rund 235 Tage lang im Beutel und noch weitere 130 Tage bei Fuf§ gesaugt. Der verzdgerte Cyclus der Fortpflanzung kann also wahrend und auch lange vor Beendi- gung der Laktation auftreten. Normaler Cyclus der Fortpflanzung tritt auf, wenn kein Junges im Beutel ist. Die Lange von normalen und verzdgerten Cyclen der Fortpflanzung bei sdugen- den 2Q mit einem bzw. zwei Jungen bei Fuf$ wurde mit solchen bei nicht sdugenden Kontroll- QQ verglichen. Die Ergebnisse waren: Normaler Cyclus der Fortpflanzung bei QQ, die 1 Junges bei Fuf$ saugten: 6 Cyclen waren nicht besonders verschieden von den Kontroll-29. Zwei Cyclen waren bedeutend langer; bei einem davon machte der Embryo eine Ruhepause von etwa 7 Tagen durch. Im ganzen 8 Cyclen. Bei QQ, die 2 Junge bei Fuf saugten: 3 Cyclen nicht besonders verschieden von den Kon- troll-OQ; 2 Cyclen bedeutend langer als bei den Kontroll-QQ mit Ruheperioden des Embryos von 6 und 14 Tagen. Im ganzen 5 Cyclen. Verzogerter Cyclus der Fortpflanzung bei QQ, die ein Junges bei Fuf sdugten, ergab sich kein EinflufS des Saugens. Im ganzen 5 Cyclen. Bei QQ, die 2 Junge bei Fuf§ sdugten, war 1 Cyclus nicht sehr verschieden von den Kontroll- QQ. 5 Cyclen waren langer als bei den Kontroll-99, bei denen die Ruhezeit der Blastocyste resp. 3, 3, 6, 11 und 22 Tage betrug. In letzteren beiden setzte die Weiterentwicklung nicht ein, bevor nicht eines der Jungen weggenommen wurde. Im ganzen 6 Cyclen. Die Beobachtungen zeigten, da QQ mit 2 Jungen bei Fufs ihre Jungen doppelt so lange sdugen, wie sie ein einziges gesaugt haben wiirden. Daraus wurde geschlossen, dafs der Sauge- Stimulus, von einem oder zwei Jungen bei Fuf§ ausgeldst, sowohl die Ruhephase wahrend der Laktation, als auch die damit gleichlaufende Ruhephase des Embryos einleitet und erhalt. Die bisherige Erfahrung lift annehmen, da der Stimulus, der den Beginn der Ruhephase bewirkt, tactil ist und iiber die Zitze empfangen wird, und dafi der verzdgerte Cyclus der Fortpflanzung auftritt, oder der unterbrochene normale Cyclus wieder aufgenommen wird, wenn der Sauge- reiz sich vermindert. Einige von anderer Seite veréffentlichte Daten tiber Trichtigkeitsdauern von Beuteltieren enthalten offenbar Fehler, da die betreffenden Autoren die Bedeutung gleichlaufenden Saugens nicht beachteten. Mitgeteilte Falle, daf§ Q Beuteltiere auch nach langer Isolierung vom @ war- fen, kann ohne weiteres durch das Auftreten des verzogerten Fortpflanzungs-Cyclus erklart werden. Literature Carson, R. D. (1912): Retarded development in a red kangaroo; Proc. zool. Soc. Lond. 1912, 234-235. — Hartman, C. G. (1923): The oestrous cycle in the opossum; Am. J. Anat. 32, 353-421. — Hepicer, H. (1958): Verhalten der Beuteltiere (Marsupialia); Handbuch Zool. 8, 18 Lief 10(9), 1-28. — Hut, J. P., and O’Donocuug, C. H. (1913): The reproductive cycle in the marsupial Dasyurus viverrinus. Quart. J. micr. Sci. 59, 133-174. — Hucues, R. L. (1962): Reproduction in the macropod marsupial Potorous tridactylus (Kerr); Aust. J. Zool. 10, 193-224. — Morris, D., and Jarvis, C. (Eds.) (1959): The International Zoo Year Book, Vol. 1; London. — Owen, R. (1839-47): Marsupialia; In: The Cyclopaedia of Anatomy and Physiology, Vol. 3 (ed. R. B. Todd), London. — Pitton, P. E., and SHarman, G. B. (1962): Reproduction in the marsupial Trichosurus vulpecula. J. Endocrin. 25, 119-136. — SHARMAN, G. B. (1954): Reproduction in marsupials; Nature, Lond. 173, 302-303. — SHARMAN, G. B. (1955): Studies on marsupial reproduction. 3. Normal and delayed pregnancy in Setonix brachyurus; Aust. J. Zool. 3, 56-70. — SHARMAN, G. B. (1962): The initiation and maintenance 234 20 G. B. Sharman of lactation in the marsupial Trichosurus vulpecula; J. Endocrin. 25, 375-385. — SHARMAN, G. B. (1963): Delaved implantation in marsupials; In: Delayed implantation (ed. A. C. En- ders), Chicago. — SHARMAN, G. B., and Carasy, J. H. (1964): Reproductive behaviour in the red kangaroo in captivity; C.S.I. R. O. Wildl. Res. 9 (in press). — SHARMAN, G. B., and Pitton, P. E. (1964): The life history and reproduction of the red kangaroo (Megaleia rufa). Proc. zool. Soc. Lond. 142 (in press). — TyNDaALE-BiscoE, C. H. (1963): The rule of the corpus luteum in the delayed implantation of marsupials; In: Delayed implantation (ed. A. C. Enders), Chicago. Author’s address: Dr. G. B. SHARMAN, C. S. I. R. O. Division of Wildlife Research, Canberra, A.C. T., Australia 235 BIOLOGY OF REPRODUCTION 4, 344~—357 (1971) Rodent Pheromones’ F. H. BRONSON Department of Zoology, The University of Texas, Austin, Texas 78712 Received September 9, 1970 Social interactions, particularly among mammals, are often of a complex nature involving many specific cues and more than one sensory modality. An obvious challenge is the unraveling of such an array of stimuli and effects in order to elucidate specific stimulus-response systems; 1.e., precisely de- fined cues operating through particular Teceptors to bring about known physio- logical events. One area of research that shows promise of being a rich source of such systems is that involving the chemical- olfactory modality. Olfactory signals are of widespread usage among mammals and as- sume maior roles in a great many species. With respect to reproduction, it is now known that olfactory-mediated stimuli not only play a large role in the transfer of information that must necessarily precede insemination but that odors may also have relatively direct effects on anterior pituitary function itself. Male odors, for example, may alter the release of FSH, LH, ACTH, or prolactin in recipient females. There is the distinct possibility that precise identification of such compounds may well provide some of the best tools for elucidating the brain mechanisms and pathways normally acting as intermediaries between the environment of an animal and its reproductive behavior and physiology. The general purpose of this paper, then, is to review the subject of mammalian pheromones, particularly as they interact with reproductive processes. The bulk of experimental evidence on_ this subject concerns rodents with considerably 1This investigation was supported by Public Health Grant HD-04149 from the National Insti- tute of Child Health and Human Development. less experimentation outside of this order. Furthermore, the one species most heavily studied has been the house mouse. We can, therefore, most profitably discuss phero- monal functions within the framework of this one species supplementing the emerging generalities with information from other rodents when possible. The term pheromone has been commonly used for externally voided substances that convey information between members of the same species. While known to exert their effects via olfaction, ingestion, and possibly absorption in insects (Barth, 1970), the prime and possibly the exclusive pathway used in mammals apparently involves odors and olfactory reception. Two general types of pheromones, modelled after entomological constructs, have been commonly recognized in mammals: (a) signalling pheromones that result in a more or less immediate change in motor activity on the part of the recipient animal and (b) priming pheromones that trigger neuroendocrine and endocrine activ- ity. The response to a signalling pheromone (e.g., a Sex attractant) may be positive or negative or there may be no response at all. A response, if it does occur, will be be- havioral and is most apt to occur shortly after reception of the information. An example of a primer is a factor in male urine, the smell of which passively induces gonadotropin release in females and culmi- nates in estrous behavior 48-72 hr later. Thus the two types of pheromones may both result in changes in behavior; however, in the case of the primer, the behavioral change is considerably delayed and requires hor- monal mediation. 344 236 RODENT PHEROMONES Informational content has been experi- mentally confirmed for several odor sources in mace: urine, preputial glands, coagulating glands, and plantar glands. Suspected sources should certainly include feces, generalized skin odors, nonspecialized sebaceous glands, sex accessory glands in addition to the coagulating glands, as well as Harderian, lacrimal, and submaxillary glands. Two problems seem paramount when discussing pheremonal function in mice regardless of the source of the odor: (a) no pheromone has beer: isolated and identified and (b) the term pheromone may even be misleading in many situations in which olfactory cues are known to be used. With respect to the latter problem, a prime function of odors among mice 1s certainly identification of species, sex, sexual state, and even individual. Sev- eral experimental studies utilizing condi- tioning techniques and good stimulus control have verified that mice can make such discriminations based solely on olfactory cues and, additionally, can even detect the difference between two members of the same highty inbred strain (Bowers and Alexander, 1967; Chanel and Vernet-Maury, 1963; Kal- kowski, 1967). The same general type of experiment has been successfully accom- plished using rats but with less control over spectiic sensory modalities (Husted and Mc- Kenna, 1966). In all probability there is no such thing as a single pheromonal compound specrfically tailored for individual recogni- tion. Olfactory discrimination between indi- viduals would more reasonably seem to involve the widest possible spectrum of odor sources and to include variations in both concentration and type of odor. Whether or not such individual recognition may be thought of as having a pheromonal basis (as opposed to simply the use of a variety of olfactory cues) depends upon the definition of the term pheromone (Gleason and Rey- nierse, 1969; Kirschenblatt, 1962; Whitten, 1966). It would seem most profitable to restract the use of this term to situations 345 where there seems a reasonable probability of isolating one or at least a_ restricted , mixture of compounds that could, in turn, be synthesized and whose actions could then be reconfirmed experimentally. Secondly, it would seem necessary that any response to a pheromone should serve a_ reasonable biological function in a natural population. Following the first aspect of this argument, then, it is doubtful that the term pheromone can realistically have merit when referring to the melange of odors probably used in in- dividual identification. Likewise, it is ques- tionable if the term is useful when concerned with the probably large variety of animal odors that could influence the result of many psychological testing procedures (e.g., open- field emotionality and maze-running) unless the behavioral side of this can be more closely allied with a more naturalistic func- tion (e.g., Douglas, 1966; Whittier and McReynolds, 1965). Table 1 summarizes pheromones postu- lated for mice by various authors, 1.c., the table actually presents a series of be- havior patterns or physiological results which involve olfactory cues and in which both of the restrictions discussed previously seem possible of satisfaction. Since no pheromones have been isolated, the table can obviously only be used as a ‘best guess” for further research. Nevertheless the evi- dence for the probable existence of phero- mones seems good for some of these effects. A postulated fear substance, for example, 1s based upon evidence that mice who are stressed by blowing air upon them, or by TABLE 1 POSTULATED MOUSE PHEROMONES Signalling pheromones: Priming pheromones: }. Fear substance 1. Estrus-inducer 2. o' sex attractant 2. Estrus-inhibitor 3. © sex attractant 3. Adrenocortical acti- 4. Aggression-inducer vator 5. Aggression-inhibitor 237 346 electroshock, excrete urine whose smell causes avoidance by other mice ot which otherwise interferes with conditioning ex- periments (Carr, Martarano, and Krames, 1970; Muller-Velten, 1966; Sprott, 1969). Mice do learn to cease avoiding such odors after a period of time thus confirming the typical Jack of stereotypy of mammalian responses to signalling pheromones. Im- portantly the phenomenon is species specific as tested within a three-species framework (Muller-Velten, 1966). Rats are also known to discriminate between the urine of shocked and unshocked rats (Morrison and Ludvig- son, 1970; Valenta and Rigby, 1968). It seems reasonable, then, to suspect a rela- tively specific signalling pheromone in the urine of stressed animals which would func- tion to communicate danger to other mem- bers of the same species in a natural popula- tion. The presence of sex attractants 1s in- completely documented in mice. A female- originating pheromone acting as an_ at- tractant for males is listed in Table 1 largely on the basis of so many studies in other rodents (for rats, Carr and Caul, 1962; Carr et al., 1966; Carr, Krames, and Castanzo, 1970; Carr, Wylie, and Loeb, 1970; Le- Magnen, 1952; Stern, 1970; for voles, God- frey, 1958; and for deermice, Moore, 1962). The opposite attraction, however, is better documented. Female mice become more active when in the presence of odor drawn from a cage of males (Ropartz, 1968a), and, additionally, Scott and Pfaff (1970) have shown that females prefer urine collected from intact males to that obtained from castrates. The male’s preputial gland lipids have been implicated in this phenomenon (Bronson, 1966; Bronson and Caroom, 1971; Gaunt, 1968), with one report of such pheromonal activity in the free-fatty acid fraction (Gaunt, 1968). Considerable chem- istry has been done on the normal male gland (Sansone and Hamilton, 1969; Spener et al., 1969), and it is probable that this will F. H. BRONSON be the first mouse pheromone to be isolated and identified. A word of caution is neces- sary, however, concerning the concepts of attraction and arousal as determined in the laboratory. What is actually known, with respect to the preputial gland, is that saline homogenates or lipid extracts of these glands are preferred by females in a two- or four-choice test situation and, additionally, that such preparations will more or less instantly awaken females from a sound sleep. It is not known, for example, whether the preputial lipids are attractive to both sexes nor is it known how other species react to them. Interestingly enough, there is a sugges- tion that the attraction for male urine may actually be stronger among diestrus females than for those in estrus (Scott and Pfaff, 1970). Additionally, the preputial gland has been implicated in male aggression (Mc- Kinney and Christian, 1970; Mugford and Nowell, 1970b). Thus, while there can be little doubt that the male’s preputial contains one or more lipids acting in an informational context, the exact content of the message 1s still highly questionable. Both ‘‘aggression-inducing” and “ag- gression-inhibiting”’ pheromones have been postulated in mice. The basis for assuming the presence of an inhibitor is the fact that males whose fur has been rubbed in female urine are not attacked as frequently as expected (Mugford and Nowell, 1970a). The general repellent action of the odor of one male upon another has been known for some time (Chanel and Vernet-Maury, 1963) and several workers have shown that the odor of strange male urine will elicit attack among normally compatible groups of males. Techniques for demonstrating this latter phenomenon have included the use of soiled bedding (Archer, 1968) and rubbing urine from a strange male onto the fur of one member of a usually or expected compatible pair of males (Mackintosh and Grant, 1966; Mugford and Nowell, 1970a). In addition, Ropartz has shown the lack of 238 RODENT PHEROMONES both attack and response to attack in anosmic males (Ropartz, 1968b). Strange male urine is decidedly more effective in eliciting attack if obtained from an intact rather than from a castrate male (Mugford and Nowell, 1970a). Androgenized females elicit considerable aggression from normal males and it has been suggested (a) that these females were producing an androgen- dependent pheromone that resulted in attack and (4) that the preputial gland is the source of this pheromone (Mugford and Nowell, 1970b). Somewhat confusing, but indicative of the importance of the preputial gland, is the report that preputialectomized males fight more frequently than expected when housed with intact males (McKinney and Christian, 1970). There can be little doubt, then, that mice make ready use of urinary signals, and possibly a specific androgen- dependent pheromone from the preputial gland, in their assessment of a potentially ageressive encounter. A correlated behavioral iesult of exposure to strange male odor is a genera! increase in motor activity. Importantly, no increase in activity is found if a group’s own odor is passed back onto themselves in a control experiment (Ropartz, !967a). Ropartz has implicated two odor sources in the activity change: a urinary factor traceable to the coagulating glands and a secretion by the plantar glands in the soles of the feet (Ropartz, 1967a). The former is apparently produced only among males found in groups while the latter is thought of as a type of individual identification. Of particular interest within this context is a possible primer effect; strange male odor causes an increase in adrenal weight and a decrease in adrenal ascorbic acid among isolated male mice (Archer, 1969; Ropartz, 1966). Ether extracts of coagulating glands cause an in- crease in adrenal weight (Ropartz, 1967a), but odors from cages of females also increase adrenal weight in males (Ropartz, 1967b). The full story on these interesting observa- 347 tions is, of course, yet to come, but the need to precisely measure changes in activity and aggression as well as to investigate the possible adrenal-activating primer at the same time in the same experimental program is obvious. In summary of the status of mouse signal- ling pheromones, then, it can be said that experimental evidence is slowly accumulating to support the common sense concept that nocturnal animals rely heavily on signalling pheromones and olfactory reception for much of their social communication. Addi- tionally, considering the manifold types of information possible or necessary in a mouse population, it can be expected that odors will be experimentally implicated in many other behaviora] dimensions. Elucidation of both the chemistry and the correlated behavior of these phenomena should prove an inter- esting future area of research. The major interest in pheromones for reproductive physiologists has been within the framework of the priming cfects dis- covered since 1955. These odors have potent and obviously interesting effects: inducing or inhibiting estrus and ovulation, accelerating sexual maturity in young females, and block- ing implantation (recent reviews include Bronson, 1968; Bruce, 1966, 1967, 1970; Gleason and Reynierse, 1969; Whitten, 1966; Whitten and Bronson, 1970). One of the best documented aspects of primer pheromone function :n mammuals is certainly in the control of the laboratory mouse estrous cycle. While typically thought of as possessing 4 to 5-day periodicity, cycles ranging up to 11-12 days may be easily produced and should be considered perfectly normal depending upon the olfactory en- vironment in which the females are housed and the strain under consideration (Bronson, 1968). Two different phenomena interact to produce such variation: (@) the suppression of estrous cycling by a poorly understood odor that is produced among groups of females and (b) the acceleration or induction 239 348 of cycling by a factor in male urine. Cycles of relatively short duration, then, are ob- tained in some but not all strains by isolation or, in most strains, by exposure to male odor. Longer cycles result from grouping of fe- males in the absence of any male odor. All- female suppression of estrus may take the form of a prolonged diestrus (Whitten, 1959) or spontaneous pseudopregnancy (van der Lee and Boot, 1956) and is only in- directly correlated with adrenocortical ac- tivity (Bronson and Chapman, 1968). The evidence that a priming pheromone is in- volved rests largely on reports that such suppression is alleviated by olfactory bul- bectomy and is independent of vision, audi- tion, and physical contact (Bianchifiori and Caschera, 1963; Mody, 1963; van der Lee and Boot, 1956; Whitten, 1959). The presence of a pheromone has been better established as the stimulus associated with a male that can override the suppressive effects of all-female grouping and, hence, synchronize the attainment of estrus among a sroup of females (Whitten, 1956a). Malic urine of the appropriate species induces estrous synchrony in both mice and deer- mice (Bronson and Marsden, 1964; Marsden and Bronson, 1964). The mouse pheromone is apparently of small enough molecular size to be transported at least eight feet on a 0.25-mph air current (Whitten ef al., 1968). Additionally, it has been shown that just the presence of males in the same animal room is sufficiently stimulating to influence cycle duration in wild house mouse females (Chipman and Fox, 1966). Bladder urine has proven as effective in inducing estrus as externally voided urine, thus apparently ruling out the possibility that the preputial attractant and the estrus-inducing primer are the same compound (Bronson and Whitten, 1968). It should be noted here, however, that one Jaboratory has reported a relatively small but consistent degree of estrus induction by preputial homogenates (Albrecht, 1967; Gaunt, 1968). Several F. H. BRONSON possibilities exist for clarifying this apparent discrepancy; e.g., the preputial gland could concentrate to a small degree the particular pheromone under consideration or there may not be a highly specific pheromonal compound at all, only a mixture of odors all denoting a male and to which the female reacts. Important in this respect is the fact that the deermouse shows both the all- female grouping phenomenon and estrus induction by male urine, yet has no prepu- tial glands (Bronson and Marsden, 1964). On firmer ground is the fact that the pher- omone is either an androgen metabolite or the product of androgen-maintained tissue since castration removes it from urine and testosterone replacement returns it to cas- trates of either sex (Bronson and Whitten, 1968). Saline homogenates of mouse testes are ineffective in inducing estrus (Bronson, unpublished observations). An active frac- tion of urine has been obtained from a Sephadex column, but isolation and identifi- cation have not yet been accomplished (Whitten, persoual communication). A recent experiment determined threshold amounts of male urine necessary for estrus induction in deermice and two types of house mice, a wild stock and the highly inbred SJL/J strain. The results of this experiment may be used to demonstrate variation in the effectiveness of the urine- estrus response and to evaluate sensitivity to priming pheromones in general. The basic procedure involved exposing cages con- taining 8-10 adult females to one of various doses of male urine for 3 days and assessing the results by vaginal smears on the 3rd and 4th mornings. Females were tested only after a minimum of 2 weeks maintenance in clean cages in a male-free room to maximize the suppression of their estrous cycles. Fresh male urine was diluted appropriately to 10 ml (per cage to be tested) with saline mixed with antibiotic and an antioxidant (propyl gallate). Delivery of urine to females’ cages was by way of syringe pumps with attached 240 RODENT PHEROMONES timers set to deliver 0.42-ml aliquots once every hour. Polyethylene tubing connected the 10-ml syringes to a Pasteur pipette taped to the wire lid of each cage. Urine, saline (control dose), and/or urine-saline dilutions thus ran down the inside of each cage onto the females’ bedding once every hour. Deer- mouse females were tested with urine col- lected from mature males of the same species. Urine for testing both wild house mouse and SJL/J females was obtained from mature males of a stock resulting from crossing eight inbred lines of laboratory mice. Doses of urine tested for the three types of females and results are shown in Fig. 1. Numbers of females represented by each point in Fig. 1 ranged from 40-60 for deer- mice, 38-80 for wild house mice, and 39-75 for SJL/J females. Lowest doses at which a Significantly increased incidence of estrus occurred were 0.01, 0.1, and | ml/day/cage of females for deermice, wild house mice, and SJL/J females, respectively (p < 0.01 in each casc when compared to control cages receiving only saline—antibiotic—antioxidant mixture). Estrus was thus induced in some female deermice by adding as little as 0.01 ml of male urine per day for a 2-day period to their bedding. Importantly, this response was set against a background of the pre- sumably inhibiting odor typical of closely confined groups of females. At the other extreme was the lack of response among the inbred SJL/J females at doses lower than 1 ml/day; a quantity not much less than the output of a normal male in a 24-hour period. Whether or not such differences are traceable to quantitative differences in pheromone be- tween the two types of urine or to the level of sensitivity of the female is, of course, unknown. It should be noted, however, that the comparison of the deermouse dose-re- sponse curve with those of the two types of house mice is somewhat suspect since deer- mouse females repeatedly chewed off the ends of the glass pipettes through which urine was being delivered in all cages tested 349 %e FEMALES in ESTRUS /2 DAYS 9 0.001 oKe)| ‘OH ) 2 4 10 DOSE of MALE URINE (ml/cage/day) FIG. 1. Estrus-induction by dripping various doses of urine onto the bedding of cages con- taining deermice, SJL/J inbred mice, or wild house mice. (See text for explanation.) at or above 0.01 ml/day. This brings up the interesting possibility of a sex attractant in deermouse male urine but does somewhat negate comparison of responsiveness; 1.e., deermice were obviously being directly smeared with urine during their chewing activities. Finally it should be noted that Species specificity has been established for the urinary primer pheromone within the limited framework of deermice, another inbred house mouse strain, and human male urine (Bronson and Whitten, 1968). The picture emerging from the above studies, then, is that of a small molecule in male urine that is androgen dependent, species specific and, at least as tested in deermice in the laboratory, may act at temarkably low concentrations to initiate an estrous cycle via olfactory reception. The mechanism of action of this molecule is assumed to be by way of the hypothalamus and to cause the release of gonadotropin by the anterior pituitary. Adenohypophyseal acidophils decrease in female mice as a consequence of cohabitation with a male but at a time too late in the cycle to be a reflec- tion of the initial effect of the pheromone (Avery, 1969). Binge] and Schwartz (1969) 24] 350 examined pituitary concentrations of LH during proestrus and estrus in mice and found no difference between cycles spon- taneously initiated and those induced by the presence of males. The question of whether or not the initial action of the pheromone is to release both FSH and LH is still somewhat uncertain. Concentrations of FSH increased in both the plasma and pituitaries of ovari- ectomized females following 3 days of male exposure but changes in LH in this experi- ment were questionable (Bronson and Des- jardins, 1969). A male may be substituted for an injection of either PMS or HCG in the normal injection regime used to induce ovulation in immature mice thus arguing for a tota! gonadotropin release by the male’s pheromone (Zarrow er al. 1970). Hormonal controls on the action of the pheromone are likewise largely unknown. Bronson and Desjardins (1969) failed to find the expected change in pituitary and plasma FSH in male-exposed, ovariectomized fe- males when females were given chronic in- jections of estradiol. Even though the dosage of estradiol used was relatively low, such a finding correlates well with Whitten’s (Whit- ten, 1956a) earlier conclusions that the male is effective in inducing a cycle only when exposure takes place during metestrus or diestrus. A blockage of the release of FSH in response to the pheromone by the higher titers of estrogen at proestrus and estrus, therefore, seems at least possible. Finally, the same pheromone discussed above is undoubtedly the stimulus associated with a male that accelerates sexual maturation in young female mice since male-soiled bedding will also exert this effect (Wandenbergh, 1967, 1969). The estrus-inducing compound discussed above, coupled with individual identification, provides adequate pheromonal basis to conceptualize a block to implantation re- sulting from exposure to a strange male; a phenomenon first described in laboratory mice by Bruce (1959). Removal of the stud F. H. BRONSON from an inseminated female’s home cage and replacement with another male results in a failure to implant and a return to estrus in both mice and deermice. This effect is absent in anosmic females and may be duplicated by exposing the inseminated fe- male to pooled urine providing the urine is collected from a normally or experimentally androgenized mouse (Bruce, 1965; Bruce and Parrott, 1960; Dominic, 1965). Such a response to a male would seem to be similar to the estrus-induction phenomenon previ- ously described, given: (a) accommodation on the part of the female to the pheromones of the original stud but not to those of the stranger, and (b) the hormonal responses to male odor possibly being somewhat different in inseminated females than they are dunng metestrus or diestrus. The former supposition would seem to be of prime importance since Teexposure to the original stud male does not result in a blocked pregnancy. Addi- tionally, the efficiency of blockage is en- hanced if stud and strange males are of different strains (Parkes and Bruce, 1961). Thus the key concept would appear to be discrimination on the part of the female between the odors of the two males; a discrimination allowing her to cease re- sponding to the stud after his original im- duction of her estrous cycle but to react to the new male by hormonal changes leading to a return to estrus at the expense of i1m- plantation. Such a process implies signalling pheromonal differences (individual identifi- cation of males) as well as sensory, central integrative, and stercidal influences on the part of the female, none of which are well understood. The obvious effect of strange male exposure is to prevent functionalization of the corpus luteum. Protection from the block may be obtained by injecting prolactin concurrently with male exposure in both mice and deermice (Bronson et al., 1969; Bruce and Parkes, 1960; Dominic, 1966) Suggesting that the primary effect of the male is to enhance the normal tonic inhibi- 242 RODENT PHEROMONES tion of prolactin release. Chapman ef al. (1970), however, found a decrease in pitui- tary LH (and, hence, presumably a release of LH) preceding any effect on pituitary pro- lactin content in inseminated females as a consequence of strange male exposure. To further confuse the picture, adrenalectomy protects against the block in one stock of laboratory mice (Synder and Taggert, 1967) and greatly increased levels of circulating corticosterone have been reported in in- seminated deermice during the initial stages of strange male exposure (Bronson ef al., 1969). In the latter case, however, adrenal- ectomy offered no protection against an implantation failure and even pharmacologi- cal doses of ACTH did not decrease the probability of implantation. There is evi- dence on hand, then, that the odor of strange male urine acts at the level of the adeno- hypophysis to influence prolactin, LH, ACTH, and probably FSH also since this latter hormone is increased during normal estrus induction by urinary pheromone. One could wish at this point for assay of all four hormones in ovariectomized or immature females and in recently inseminated fe- males following exposure to the cleanest urinary preparation available. Of particular interest 1s the possibility mentioned previ- ously of a urinary primer acting on the adrenal cortex that may or may not have any effect on gonadotropin release. Given the present status of our knowledge about mouse pheromones, it is interesting to ask several questions, the first of which concerns the number of pheromones actually denoted by past experimental work. Table 1 lists five suspected signalling and_ three possible priming pheromones. The list could be expanded by assuming Ropartz’ verifica- tion of the effect of coagulating glands on general motor activity to be entirely separate from aggression induction. On the other hand, the list could be considerably short- ened by applying Occam’s razor and as- suming the brain of a recipient animal 3ol sufficiently flexible to use the same odor for different types of information and, hence, for different responses depending upon the situation. One could, for example, suspect that the aggression-inhibiting aspect of fe- male urine is a sex attractant which overrides any potential aggression. Importantly, the estrus-suppressing primer could be a labora- tory artifact reflecting high concentrations of a noxious compound in the bedding. It is known, for example, that ammonia is capable of inhibiting cycling in rats (Takewaki, 1949). Interesting in this regard is the fact that high doses of male urine are apparently ineffective in inducing estrus (see Fig. 1). Finally it could be stated that the concept of an adrenocortical activator needs further verification, particularly with respect to past social experiences of the test animals and in regard to biological function, before a Specific primer is postulated. Before grappling with the problem of the many diverse reports of olfactory-induced changes in aggression and motor activity, then, the list of potential pheromones could be considerably reduced. Likewise, it could be postulated that the compound(s) in the male’s preputial gland acting to attract females are the same that elicit aggression when perceived by another male rather than a female. An argument could also be made that increased aggression, motor ac- tivity, and adrenal function are all related to simply the perception of strangeness. Male mice when housed together normally estab- lish social hierarchies which are organized initially by fighting and often maintained thereafter by recognition of individual status in the hierarchy without overt aggression. Placing a mouse with a new individual odor among an already organized group or over- riding the odor of some individuals by rub- bing their fur with urine from strange males could certainly be expected to result in the resumption of fighting in an effort to re- organize the group. Increased adrenal func- tion is known to accompany fighting among 243 302 males (Christian, 1971) and such an effect may be prolonged in a defeated mouse (but not in an undefeated mouse) just by the presence of a dominant male without physi- cal contact (Bronson, 1967). It would thus seem that the melange of odors probably used in individual identification would be of prime importance as opposed to either a specific aggression-inducing compound or an adrenocortical-activating primer. Arguing against this unified concept are the androgen dependency of the aggression-induction sig- nal, Ropartz’ implication of the coagulating and plantar glands in activity changes, and the verification that strange male odor in- creases adrenal function in isolated males. Since not all odors associated with males are androgen dependent, one must almost postu- late an androgen-dependent, core compound that carries the message ‘‘male” with in- creased activity and aggression being par- tially determined by the relative strangeness of the melange of associated odors. A similar concept has been applied by Whitten (1966) to conceptualize the pheromonal block to pregnancy by strange males. It could even be that one androgen-dependent compound occurs in both the preputial and the coagulating glands and, hence, leads to both glands being postulated as sources for effects on aggression and general motor activity. Finally, it should be noted that the fear and aggression-inducing reactions to male urine have been conceptually linked in mice by Carr, Martarano, and Krames (1970), who used both electroshock and physical defeat as stressors in the same study. These workers showed that the odor of a trained fighter is different from that of a trained loser and, secondly, that animals of different past social experiences may react differently to the two types of odors. There is thus the possibility that mice might secrete a urinary product that would vary in con- centration with dominance status. Further- more, since low ranking animals are com- monly in a stressed condition, the urine of a F. H. BRONSON subordinate might be similar in some re- spects to the urine of a physically stressed animal. Some interesting speculations arise since both adrenal and testicular function are known to be altered by subordination and presumably, by electroshock treatment. Nevertheless, the key concept in aggression induction would still seem to be detection of first a male odor and, secondly, a strange- ness and it is difficult to visualize this aspect of an animal as being denoted exclusively by a single compound varying in concentra- tion. A signalling pheromone associated with social dominance has been suggested for rats (Krames et al. 1969). Regardless of how future research re- solves the above problems, it is probable that, as of this time, we are not justified in postulating as many specific pheromones as are listed in Table 1. A more realistic lst would include three signalling pheromones and one primer: (a) a fear substance; (6) a female originating signal which both at- tracts males and blocks attack when strange- ness is detected; (c) a male-originating signal that attracts females and, when coupled with the many odors denoting strangeness, leads to aggression; and (d@) a single primer that induces estrus, ac- celerates the attainment of sexual maturity, and when coupled with strangeness, wall induce estrus at the expense of implantation. A possible adrenocortical-activating primer is particularly interesting but needs further elaboration with respect to its function and interaction with other pheromones. A second question concerns what might be expected in terms of pheromone chem- istry. First of all the signalling—primmg dichotomy is useful for discussing phero- mone function but may be inadequate in terms of chemistry; i.e., one pheromone could serve both functions. Secondly, the one reasonably well isolated mammahan pheromone, that of the tarsal gland of black-tailed deer, is apparently a decided mixture of compounds (Brownlee ef al., 244 RODENT PHEROMONES 1969; Muller-Schwarze, 1969). The major component causing licking and sniffing by other deer is cis-4 hydroxydodec-6-enoic acid lactone but several other lactones in the gland also result in this behavior and it is probable that the normal pheromone is a mixture of several lactones. Should mixtures prove common for mammalian pheromones, chemical isolation and identification with correlative biology will prove more difficult. On the other hand the pheromone in the boar’s preputial gland, which acts on estrous females (Dutt et a/., 1959; Signoret, 1970; Signoret and deBuisson, 1961), might prove to be a simple androgenic steroid like andros-16-en-3-0l which structurally re- sembles civetone and muskone (Katkov and Gower, 1968; Sink, 1967). The latter possibility is intriguing for mouse phero- mones because of the verification of andro- gen dependency for the sex attractant, ag- gression-inducer, and estrus-inducing primer. The probability of a high degree of species specificity in pheromones, however, argucs against the widespread use of the more typical androgen metabolites as pheromones. A question that is always paramount in biology is the generality of phenomena across species. Anecdotal information confirms the wide use of olfactory signals for a variety of communicative purposes in mammals (e.g., Wynne-Edwards, 1962), Reasonable verifica- tion of probable primer effects has been limited to reproductive phenomena and, additionally, to only mice, deermice, and two species of voles. Deermice, Peromyscus maniculatus, show all-female suppression as well as both the estrus-inducing and preg- nancy-blocking actions of male urine (Bron- son and Dezell, 1968; Bron and Marsen, 1964; Elefteriou et al., 1962). The vole, Microtus ochrogaster, an induced ovulator, rarely cycles unless placed in the presence of males or male-soiled bedding, or when disturbed by cage changings (Christenson and Gier, 1971; Richmond and Conaway, 1969). Another vole, M. agrestis, shows the 353 strange male implantation block although olfactory mediation has not yet been verified (Clulow and Clarke, 1964). It seems not un- reasonable to expect that the use of priming pheromones has much wider usage among mammals than that now documented. Male induction of estrus is known in some other Species even through the exact sensory modality in use is unknown (e.g., the desert pocket mouse, Perognathus penicillatus, Wilken and Ostwald, 1968). Probably there is no way at present to generalize about the use of pheromones, priming or signalling, among mammals. Female mice of some strains cease cycling entirely following anos- mia (Whitten, 1956b) while other species show only minor effects of the loss of the sense of smell (e.g., guinea pig, Donovan and Koprina, 1965). Surprisingly, the rat may well prove to be a typical, or average, mammal in this respect. Barnett (1963) has documented the importance of olfactory communication in wild rats. The rat’s ability to display sexual behavior, however, is not completely dependent upon any one sensory modality (Beach, 1947). Experi- mental anosmia may result in some degree of depression of sexual behavior (Bermont and Taylor, 1960) but strong, direct effects of olfactory lobectomy appear only when combined with loss of another sensory modality; for example, puberty is delayed in female rats by a combination of anosmia and blinding but not by either procedure alone (Reiter and Ellison, 1970). Further- more, a possible primer effect has been documented in the rat, the induction of estrus by a male (exact modality used is unknown), but this effect occurs only under conditions of starvation (Cooper and Haynes, 1967). The pregnancy-blocking re- sponse could not be demonstrated in rats (Davis and de Groat, 1969) but incidence of spontaneous pseudopregnancy is apparently influenced by social conditions (Alloiteau, 1961; Everett, 1963). In other words, the rat apparently does utilize olfactory stimuli to 245 304 Support its reproduction and sexual be- havior but is far from being dependent upon them as long as other sensory modalities are operative. In all probability, there will prove to be many species like the rat just as there are probably many that heavily utilize pheromones, priming and signalling, and some species relatively divorced from such communication. Finally, it is interesting to speculate that, in addition to finding many more species utilizing priming pheromones, we could also expect to find their interaction with other aspects of reproductive physiology. A largely unexplored area of research is that dealing with early olfactory imprinting (e.g., Main- ardi, 1963). A third type of pheromone classification has been evolved to cover this phenomenon in which early exposure to odors permanently alters the nervous system in terms of adult response to odors. Other possible areas of research include the re- sponse of the lactating female to odors. Maternal behavior is completely absent in anosmic mice (Gandelman ef a/., 1971) and nonsocial odors have been shown to in- fluence milk ejection in rats (Grosvenor and Mena, 1967). REFERENCES ALBRECHI, E. D. (1967). Source of the pheromone causing estrous synchronization in the laboratory mouse. Thesis, University of Vermont. ALLOITEAU, J. J. (1961). 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Fert. 23, 357-360. 249 REPRODUCTION AND GROWTH IN MAINE FISHERS’ PHILIP L. WRIGHT, Montana Cooperative Wildlife Research Unit and Department of Zoology, University of Montana, Missoula MALCOLM W. COULTER, Maine Cooperative Wildlife Research Unit, University of Maine, Orono Abstract: New data concerming reproduction, aging techniques, and growth of fishers (Martes pennanti) were obtained from 204 specimens taken from October to April during 1950-64. All female fishers more than 1 year old were pregnant. The immature class consisted of juveniles in their first year. The period of delayed implantation lasted from early spring until mid- or late winter. Nine adult females taken in January, February, or March showed implanted embryos. Fishers in active pregnancy had corpora lutea 7 times the volume of those in the period of delay. Most litters are born in March, but some as early as late February and some in early April. Counts of corpora lutea of 54 animals taken during the period of delay and during active pregnancy averaged 3.35 per female. The number of embryos, either un- implanted or implanted, corresponded exactly with the number of corpora lutea in 18 of 21 animals. Two recently impregnated l-year-old females, recognizable from cranial characters, had tubal morulae, confirming that females breed for the first time when 1 year old. Also confirmed are previous findings of Eadie and Hamilton that juvenile females can be distinguished from adults by open sutures in the skull throughout their first year. Juvenile males can be recognized in early fall by open sutures in the skull, absence of sagittal crest, immature appearance and lighter weight of bacula, unfused epiphyses in the long bones, and small body size. The sagittal crest begins to develop in December and often is well developed by March. The baculum grows slowly during the early winter, but by February there was some overlap with weights of adult bacula. Male fishers showed active spermatogenesis at 1 year. Open sutures were found in juvenile male skulls throughout the first year. Pelvic girdles of juveniles were distinguished by an open pubo-ischiac symphysis; adults of both sexes showed the two innominates fused into a single bone resulting from at least a partial obliteration of the symphysis. Mean body weights of animals weighed whole in the laboratory were as follows: adult males, 10 Ib 12 0z; juvenile males, 8 Ib 74% oz; adult females 5 Ib 8 oz; juvenile females, 4 lb 11 oz. After reaching an all-time low during the early part of the century, the fisher has made a remarkable recovery during the past 25 or 30 years in Maine (Coulter 1960) and in New York State (Hamilton and Cook 1955). The increase in abundance of this 1This study is a contribution from the Maine and the Montana Cooperative Wildlife Research Units, the University of Maine, the Maine De- partment of Inland Fisheries and Game, the Uni- versity of Montana, the Montana Fish and Game high quality furbearer in New York to the point that it could be legally trapped al- lowed Hamilton and Cook (1955) and later Eadie and Hamilton (1958) to discover sig- nificant facts from studying carcasses ob- tained from trappers. Department, the U. S. Bureau of Sport Fisheries and Wildlife, and the Wildlife Management In- stitute cooperating. The study was supported by Grant GB-3780 from the National Science Foun- dation. 250 In Maine, the season was reopened in 1950, permitting collection of data and ma- terial from fishers trapped there. The pur- pose of the present paper is to present new information about reproduction, age de- termination, and growth of fishers, derived from study of Maine animals obtained be- tween 1950 and 1964. More than a dozen biologists and many wardens of the Maine Department of In- land Fisheries and Game collected material from trappers. Special thanks are due to Myron Smart, Biology Aide, who assisted in numerous ways throughout the entire study, and to Maynard Marsh, Chief Warden, who made arrangements for confiscated speci- mens to be processed at the Maine Unit. Numerous graduate assistants at the Maine Unit helped with processing carcasses and the preparation of skulls and bacula. We are indebted to Howard L. Mendall for edi- torial assistance and to Virginia Vincent and Alden Wright who made the statistical calculations. Margaret H. Wright did the microtechnique work. Elsie H. Froeschner made the drawings. Some of these findings were summarized in an unpublished Ph.D. dissertation presented by Coulter at the State University College of Forestry at Syracuse University. FINDINGS OF PREVIOUS WORKERS Hall (1942:147) published data from fur farmers in British Columbia showing that the gestation period in captive fishers ranges from 338 to 358 days and that copu- lation normally takes place about a week after the young are born. Enders and Pear- son (1943) described the blastocyst of the fisher from sectioned uteri of trapper-caught animals and showed that the long gestation period is due to delayed implantation. It was assumed that the blastocysts remain in- active from spring until sometime during winter. De Vos (1952) studied fishers in MAINE FisHers ¢ Wright and Coulter 71 Ontario and made preliminary attempts to establish an aging method based upon skulls of males and females and the bacula of males. Hamilton and Cook (1955) pub- lished information about the current status of fishers in New York State and described a technique for recovering the unimplanted blastocysts from fresh reproductive tracts by flushing them out with a syringe. Eadie and Hamilton (1958) provided additional data on the numbers of blastocysts in preg- nant tracts and described cranial differ- ences between adult and immature females. MATERIALS AND METHODS Coulter collected material in Maine from trapped fishers, starting in 1950 when the season was first reopened. The intensity of the collection varied over the years depend- ing upon the legal regulations in effect. Data are available from 204 animals. In addition to animals legally taken dur- ing the trapping season, Coulter obtained a number of animals both before and after the season, taken by trappers who were trapping other species, primarily bears and bobcats. Trappers who caught fishers ac- cidentally were required to turn them over to the Department of Inland Fisheries and Game which in turn brought or sent them to the Maine Unit at Orono where they were autopsied by Coulter. Unskinned fish- ers as well as skinned carcasses were sub- mitted to the laboratory. Whenever possi- ble, weights were taken immediately before and after skinning to obtain an index for converting the weights of carcasses re- ceived from trappers to whole weights. During the trapping season carcasses were collected at trappers’ homes. Usually the material was submitted in fresh condition; often it was frozen or thoroughly chilled when received at the laboratory. Because of the interest of the cooperators, most of the material was accompanied by collection 251 Te Journal of Wildlife Management, Vol. 31, No. 1, January 1967 dates, method of capture, locality, and other notes. These data together with measure- ments, weights, observations about the con- dition and completeness of the specimens, and a record of material saved for future study were entered on individual cards for each animal. A special effort was made from the fall of 1955 to the spring of 1958 to obtain com- plete skeletons, and 59 such specimens were obtained. Coulter trapped a series of espe- cially needed animals in late March and early April, 1957. Because of excellent co- operation by State Game Wardens and Re- gional Biologists, a good sample of speci- mens was available for study over a 6- month period from October to April. This series of fishers is an unusually valu- able one for discerning important aspects of the growth and the reproductive cycle of this mustelid. For example, nine females in active pregnancy were obtained, as well as several adult males in full spermatogenesis. Furthermore, the juvenile fishers were grow- ing and maturing rapidly during the col- lecting period, and this fairly large collec- tion has allowed us to reach significant con- clusions concerning the onset of sexual ma- turity and the distinction between the age classes with more assurance than de Vos (1952) was able to do with more limited material. The reproductive tracts of female fishers were removed in the laboratory and pre- served in 10-percent formalin, in AFA, or in special cases, Bouin’s fluid. The bacula of all the males were air-dried, as were the skulls of both sexes. Testes from a few rep- resentative males were fixed in formalin also. Coulter solicited the cooperation of Wright in 1955 and all of the material then available was shipped to him for further analysis and for histological work. Most of the skeletal material was cleaned by der- mestid beetles in Montana. This study was carried out without the aid of known-age specimens. Since the study was completed, three known-age ani- mals have become available: an 18-month- old female in Maine which was in captivity for 1 year, and two females captured in central British Columbia, released in west- ern Montana, and recaptured 6 years later. Study of these three animals in no way af- fects the findings presented in this paper. Evidence is presented to indicate that young-of-the-year animals can be distin- guished from adults by studying either their skulls and skeletons or their reproduc- tive tracts. Animals judged by these criteria to be less than 1 year old are, for conve- nience, referred to as juveniles even though in a few cases they may be almost 1 year old. Except for one criterion for distinguish- ing yearling females from older adult fe- males, described by Eadie and Hamilton (1958:79-81) and confirmed here, no method of determining the relative ages of adults was discovered. Wherever appropriate, standard devia- tions and standard errors have been calcu- lated, but generally such figures are not presented here. When it is stated that a significant or highly significant difference exists, it is based upon the use of the ¢ test. FINDINGS Female Reproductive Tracts The reproductive tract of the female fisher is similar to that of other mustelids. The ovaries are completely encapsulated with only a small ostium through which a small portion of the fimbria extends. The ovary must be cut free from the bursa under a dissecting scope with a pair of fine scissors. The oviduct encircles the ovary as in other mustelids. The oviducts were not highly enlarged in any animals studied, since no estrous stages were seen. The uterus has a common corpus uteri which allows embryos 252 developing in one horn to migrate to the other horn. The uterine horns are 40-60 mm long in adult females in inactive pregnancy, and 2’2-4 mm in diameter. Immature fish- ers show smaller uteri with horns about 30- 40 mm long and 1%-2% mm in diameter. No search was made for an os clitoridis. The ovaries from each preserved tract were dissected from the fixed reproductive tract, blotted, and weighed. Each ovary from animals taken in fall or early winter was sliced macroscopically and the number of corpora lutea present determined by the use of a dissecting microscope. Of the 77 tracts handled in this way, 44 animals showed corpora and were thus judged to be adults. Thirty-three animals were without corpora and were judged to be immature. The average combined weights of the ovaries was 134.4 mg for adults and 76.5 mg for immatures. The average weight of the left ovaries (I—40.3 mg, A—70.0 mg) was greater than that of the right ovaries (I—36.2 mg, A—64.4 mg) in both im- matures and adults, but no special signifi- cance is ascribed to this matter. The aver- age number of corpora lutea from this series of 44 adult females was 1.68 in the right ovaries and 1.60 in the left; the average was 3.28 per adult female. Eadie and Hamilton (1958) reported that the mean number of corpora lutea in 23 adult New York fishers was 2.72. The difference in the average number of corpora lutea between the Maine and New York samples is highly significant. The distribution of the corpora lutea from all of the Maine, pregnant animals is shown in Table 1. To determine the relationship between the number of corpora lutea in the ovaries and the number of blastocysts in the uteri, 11 tracts of adult females were studied in detail. After the ovaries were removed and sectioned by hand, uteri were selected that appeared to be the best preserved. These MAINE FIsHERS * Wright and Coulter 73 Table 1. Distribution of corpora lutea in ovaries of preg- nant Maine fishers. No. oF Cor- No. OF PORA IN CoRPORA IN No. OF BotH Ova- No. OF SINGLE CASES RIES OF FEMALES OvARIES INDIVIDUAL FEMALES 4 Py 3) 1 3} 14 4 21 2 42 3 30 i 43 ye) 2; 0) 8 — —- 54 Total 109* * One case in which only one ovary available. entire uteri were dehydrated and cleared in wintergreen oil. Study of the entire cleared tract under a dissecting scope using transmitted light often revealed the loca- tion of blastocysts. Serial sections of each of these tracts were made to locate the blastocysts. As soon as all of the expected blastocysts were found, no further section- ing of that tract was done. In some cases the entire uterus was sectioned before all the blastocysts could be located, and in 2 of the 11 tracts, 1 potential blastocyst was not found. This represents a loss of only 6 percent, as there were 35 corpora in the ovaries of the 11 animals and 33 blastocysts were located. The technique of Hamilton and Cook (1955:30-31) of flushing the uteri for the blastocysts was not followed here since the tracts had been fixed in for- malin. The sectioned blastocysts were similar to those described by Enders and Pearson (1943:286). The extremely thick zona pel- lucida, 14.4 » according to these authors, makes it possible to find the blastocysts in very poorly preserved material. None of the blastocysts studied was in better condi- tion than those seen by Enders and Pearson, and the relative numbers of nuclei in the trophoblast and the inner cell mass for this species is still not known. In order to ob- 253 74 Table 2. Journal of Wildlife Management, Vol. 31, No. 1, January 1967 Findings in nine reproductive tracts of female fishers in active pregnancy. WEIGHT OF DISTRIBUTION OF DATE OVARIES (MG) CorpoRA LUTEA STATE OF KILLED UTERUS Right Left Right Left January, 1965 — — - - 3 embryos, 18 mm CR (Crown—Rump) February 2, 1961 118 re 3 1 4 embryos, 2R, 2L, 17-mm swellings, em- bryo 8 mm CR February 7, 1956 182 98 o 0 3 embryos, 1R, 2L, embryo 13 mm CR February 21, 1964 110 73 2 1 3 embryos, 2R, 1L, embryo 18 mm CR Late February, 1959 98 108 1 3 4 embryos, 2R, 2L, embryo 8 mm CR March 3, 1959 179 138 3 1 4 fetuses, 2R, 2L, 2 males, 2 females, fetuses 53, 54, 55, 57 mm CR March 11, 1965 — — 1 3 fetuses, 2R, 1L, 3 males, fetuses 69, 71, 74 mm CR March 13, 1956 92, 92, 1 3 early embryos, 2R, 1L, 7-mm swellings March 20, 1957 OM ST il 2, 3 fetuses, 2R, 1L, 3 females, fetuses 74, 80, 83 mm CR tain such material, adult tracts would have to be preserved in a matter of minutes after the animal was killed. Tracts of nine adult fishers in which there were implanted embryos were studied (Table 2). Studies of the marten and a weasel are of some value in estimating the times of parturition in these tracts. Jonkel and Weckwerth (1963:96-97) made a series of laparotomies on late-winter adult female marten (Martes americana) and de- termined that the interval between implan- tation and parturition was less than 28 days. In the long-tailed weasel (Mustela frenata), Wright (1948) showed that the postimplan- tation period lasted about 23 or 24 days. In estimating the parturition dates from the pregnant fisher tracts it is assumed that the period of active pregnancy is about 30 days. This seems reasonable on the basis of the larger size of the fisher in comparison with the marten and the weasel. The female fisher with the largest fetuses, taken on March 20, would probably have borne young before April 1. The one with the earliest stages was taken on March 13, and it is estimated that her litter would not have been born until after April 1. The one with the 13-mm (crown-rump) embryos, taken on February 7, would have borne her young before the end of February. Two re- cently captured females produced litters on March 2 and on March 20 at the Maine Unit. The evidence indicates that the ma- jority of Maine fishers produce their litters during the month of March, but some do so as early as mid-February, and some as late as early April. The ovaries of female fishers with im- planted embryos were all serially sectioned. The ovaries are much larger than those in inactive pregnancy, the average combined weight being 231.9 mg as compared with 134.4 mg for the inactive group. The corpora lutea are markedly enlarged in active pregnancy as is generally known in mustelids with long periods of delayed im- plantation (Wright 1963:87). The corpora of three of these animals averaged 2,380, 2.917, and 3,057 » in diameter, whereas corpora from two animals with unimplanted blastocysts averaged 1,387 and 1,219 y». Al- though these corpora in animals with im- planted embryos are more than seven times the volume of those with unimplanted em- bryos, the increased size of the ovaries is not due solely to the increase in corpus size. In no case is the histological preservation of high quality, but the corpora lutea were readily seen and counted in all ovaries. 254 There is a great deal of interstitial tissue in all of these ovaries, and in this they differ from weasel ovaries (Deanesly 1935:484) in which the interstitial tissue is most active in late summer but by implantation time shows considerable degeneration. There are also numerous small and medium-sized follicles in these fisher ovaries. In all cases the cells of the corpora lutea are highly vacuolated. Vacuolated cells in corpora are common in many mustelids during the period of inactive pregnancy. Eadie and Hamilton (1958:78) noted that their fisher corpora in ovaries in inactive pregnancy were highly vacuolated. Wright and Rausch (1955:348-350) describe vacuolated corpora in the wolverine (Gulo gulo) in inactive preg- nancy, but during active pregnancy the vacuolation had disappeared. It appears then that vacuolated corpora lutea during active pregnancy is a condition not com- monly seen in this group. We suppose that the corpora lutea of active pregnancy are secreting progesterone, whereas during the inactive period there may be no active secretion of progesterone. This is suggested by the urine analysis conducted in various stages of pregnancy by Ruffie et al. (1961) on the European badger (Meles meles) which has a similar reproductive cycle. The number of embryos or fetuses in these eight animals averaged 3.38 and in each case the number of corpora lutea cor- responded to the number of embryos; that is, there was seen here no loss of potential embryos that may have occurred during either the preimplantation period or the postimplantation period. There was evidence of migration of em- bryos from one uterine horn to the other in five of the eight animals. Migration of em- bryos is well known in other mustelids. It apparently occurs largely during the process of spacing just before implantation. Only one example of migration was seen in all MaIn_E Fisuers * Wright and Coulter 75 11 tracts which were preserved during in- active pregnancy and which were sectioned to locate all of the blastocysts. On a few occasions at the time of au- topsy, Coulter observed darkened areas in the uteri which were apparently placental scars. After being fixed and cleared, most of these areas were no longer visible. Wright (1966:29) found that in the badger ( Taxidea taxus ) placental scars can readily be found in cleared tracts of parous fe- males, provided the uteri were preserved at once after death. Placental scars are diffi- cult to find, even in lactating badgers, in material that is not freshly preserved. It seems likely that the general level of preser- vation in these fisher tracts was not good enough to preserve placental scars. Breeding Season Earlier workers, Hall (1942:147), for example, indicate that the female fisher breeds soon after her litter is born; thus the gestation period may be as long as 51 weeks. Since no recently postparturient tracts were available for study, this particu lar point could not be confirmed from wild- caught animals. However, among speci- mens collected in late March and early April, 1957, two recently bred nulliparous females were obtained and the tracts pre- served fresh. These two tracts are the best preserved in the entire series, and tuba embryos were found in each by serially sec- tioning the oviducts. Each animal had three corpora lutea, 2 R, and 1 L, and 3 morulae were found in one and 2 in the other. In the one taken on March 28, one morula had about 228 nuclei (Fig. 1A); the other embryos were of comparable devel- opment, but it was not possible to count the nuclei. The animal taken on April 4 showed 2 morulae with 12 and 20 nuclei (Fig. 1B). No evidence was found of the expected 255 76 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 Fig. 1. Photomicrographs of tubal morulae from recently impregnated female fishers. from 1-year-old female taken on March 28. on April 4. third embryo. The only mustelid possess- ing a long period of delay in implantation in which the rate of cleavage is known is the long-tailed weasel (Wright 1948). If the fisher has a comparable slow rate of cleavage, the March 28 animal was impreg- nated about March 18, and the April 4 specimen was impregnated about March 27. This is probably about the same time as recently parturient females would be im- pregnated. The young developing from these tubal embryos would normally have been born about 1 year later. The ovaries of these nulliparous animals were largely masses cf interstitial tissue, apparently of cortical origin. There were no graafian follicles of medium or large size. The small, almost fully formed corpora lutea with organized connective tissue cen- ters also suggested that ovulation had oc- (Left) Embryo of about 225 nuclei, (Right) Embryo of about 12 nuclei from oviduct of 1-year-old female taken curred some 8 or 10 days earlier. The luteal cells were not vacuolated. The medulla of these ovaries was discernible only as a small area adjacent to the mesovarium. Both of these recently bred females, even though nulliparous, showed slight mam- mary development. In weasels, Wright (Un- published data) has never seen mammary development associated with the summer breeding season. The nipples become con- spicuous for the first time about the time of implantation. Both of the fishers in question were judged to be 1 year old, on the basis of the development of both their skulls and skele- tons. Another nulliparous female taken at the same time, March 27, was also judged to be 1 year old, but showed no sign of reaching estrus. This animal might have attained estrus within 2 or 3 weeks. 256 MaIn_E FisHers * Wright and Coulter 77 Table 3. Findings in tracts of male fishers taken in late winter and early spring. WEIGHT oF Com- PAIRED STATUS BINED PAIRED EpI- STATUS OF OF BACULUM EstI- DaTE TESTES TESTIS DIDYMIS SPERM IN SPERM WEIGHT MATED Bopy (1957 ) AND Epi- WEIGHT WEIGHT TESTES IN Epi- (MG) AGE OF WEIGHT a Pa (Gc) (c) DIDYMIDES ANIMAL January 5 2.7 1.8 0.4 None None 1262 Juv. 7 Ibo 3.92 February 26 7.4 5.6 1.4 Active None >? ? spermato- genesis February or early March 6.3 4.8 Te None None Nai25. Juv. 10 lb 7 oz March 1] 6.3 4.8 1.0 Active Few 252 Juv. 8 lbw 5) 0z spermato- genesis March 1 8.6 6.9 13 Abundant Abundant 1550 Juv. 9 lb 12 oz March 1-15 10.3 7.6 1.9 Abundant Abundant 1562 Adult — March 17 13 8.6 1.9 Abundant Abundant 1522 Adult Ti Ib oz March 27 7.4 5.8 1.2 Abundant Abundant 1921 Adult 8 lb 3 oz March 27 13.0 9.8 2.2 Abundant Abundant 2053 Adult 14 lb 6 oz April 4 9.0 120 Wet Abundant Abundant 1800 Adult 9 lb 5 oz Coulter has often noticed a definite change in travel pattern beginning in March and suspects that it is associated with breed- ing activities. Earlier, the animals are fairly solitary and travel in long routes in more or less direct fashion. But during March there are numerous cases of animals travel- ing together. The incidence of scent posts is much higher than in early or midwinter. At this season, reports are received of “dozens of fisher” in a given locality. Closer study shows that only two or three animals may be responsible for an unbelievable maze of tracks in a small area. In the European badger, which may also have a gestation period of almost a full year, both Neal and Harrison (1958:115- 116) and Canivenc and Bonnin-Laffargue (1963:121-122) present evidence for sterile matings occurring outside of the usual breeding season and ovulation in animals already in inactive pregnancy. Although no fishers were obtained during the period ex- tending from early April until October, it is clear from the material at hand that ovula- tion occurs only during the breeding sea- son, and there is no evidence of sterile matings. Male Tracts Since testes were generally inactive dur- ing the trapping season, they were not routinely saved from trapper-caught speci- mens. With a breeding season in March and April, it was obvious that late-winter animals would show transitional stages from the inactive early-winter condition to the active state in the breeding season. An ef- fort was made, therefore, in the late winter of 1957 to preserve testes from available males. The results of the observations are included in Table 3. The weights of the combined testes and epididymides were obtained after first stripping free the tunica vaginalis. Then the testes were further separated from the epididymides and both were weighed again. Thus, the total of the separated weights does not equal the combined weights be- cause additional connective tissue and fat had been removed. Representative sections of testes from each animal and from the 257 78 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 Figs 2. disappearance of the symphysis in a portion of the anterior half of pubo-ischiac junction. showing almost complete disappearance of pubo-ischiac symphysis. side of the symphyseal line. cartilage. eal cartilage. tail of the epididymis were prepared and stained. The juvenile male taken on January 5 was aspermatic. By late February and early March three juveniles showed somewhat enlarged testes, but only one of these ani- mals was in breeding condition. All of the adults taken from early March into early April were fully developed with abundant sperm in the tails of the epididymides. It would have been desirable to have tracts from additional males taken earlier in the winter. The results indicate, however, that adult males are fully active sexually during the breeding season; and the young males, now just 1 year old, are also apparently in breeding condition. Skeletal Development The series of 59 skeletons was studied with respect to the fusion of the epiphyses in each of the long bones and representa- tive vertebrae. Sixteen specific sites were Dorsal and ventral views of adult and juvenile fisher pelvic girdles. (A) Dorsal view of adult ¢ showing complete (B) Ventral view of adult 2 There are conspicuous rugosities projecting from each (C) Dorsal view of juvenile 2 showing complete separation of the innominates by symphyseal (D) Ventral view of juvenile @ in which the two innominates are completely separated by a substantial symphys- studied in addition to the status of fusion of the pubo-ischiac symphysis and certain sutures in the skulls. Examination of the November and De- cember skeletons showed striking differ- ences between two groups, apparently ju- veniles and adults, in both sexes. All of the sutures studied were open in November and December males judged to be juveniles; and most of the sutures were only partly closed in comparable females thought to be ju- veniles. The obviously juvenile animals were smaller and showed many open sutures in the skulls. The bacula of the males in this group were small and weighed less than 1,000 mg, compared to an average of more than 2,000 mg for those with closed sutures. The ovaries of females regarded by skeletal criteria as juveniles were all without corpora lutea; the ovaries of all those classed as adults possessed corpora lutea. The pubo-ischiac symphysis clearly re- mains open longer than most of the sutures. 258 It was completely open in all animals that were regarded as less than 1 year old taken throughout the fall, winter, and early spring. It was at least partially obliterated, when viewed either dorsally or ventrally, in all animals regarded as more than 1 year of age (Fig. 2). The findings of striking differences in the fusion of this symphysis parallel those of Taber (1956), who de- scribed differences in this symphysis ex- tending over several years in deer (Odo- coileus hemionus and O. virginianus). The pubo-ischiac symphysis should be studied in other mammals in which aging criteria are needed. Baculum Weights of bacula are shown in Fig. 3, and drawings of representative types are shown in Fig. 4. The bacula of adults are more than 100 mm long, and they com- monly weigh 2,000 mg or more. The fully mature baculum shows an elevated ridge near the proximal end that completely en- circles the bone in a diagonal line when viewed from the side. The bacula of ju- veniles taken in the fall and early winter are much smaller. Although they show the typical splayed tip at the distal end, which is universally perforated by a small, round, or oval foramen, they do not show the en- larged proximal end typical of the adults. The series of bacula in Fig. 3 shows that those of the juveniles are growing rapidly during the winter months. By February some of them weigh as much as 1,600 mg (one 2,099 mg) and thus overlap the weight of those of adults. Two such bacula are shown in Fig. 4, F and G. Since the testes of juveniles in February were becoming active, it seems reasonable to assume that such animals were secreting androgen at high levels. The fully adult baculum undoubtedly develops under the influence of androgen, MAINE Fisuers ¢ Wright and Coulter 79 26004 e @ e 24004 s r) e@ @ @ e 8 e © 22004 &e a oe ~ 20004 8 . ips ee ip) ® ) | ol z ; © 1800 lw = BACULUM 3 ° ° OcT NOV DEC JAN FEB MAR APR Fig. 3. Baculum weights. Adults are shown in solid dots, juveniles with open circles. The continued growth of the juvenile baculum during the winter months is clearly shown as is the overlap in weights of February, March, and April juveniles and adults. as it probably does in all mustelids. This was demonstrated (Wright 1950) to be the case in the long-tailed weasel. Probably the fully adult type of baculum would develop by late spring in these year-old males, since Deanesly (1935:469) concluded that the adult baculum of the European §stoat (Mustela erminea) develops to adult type within 1 month after the testes become active for the first time. Although Elder (1951:44) showed that bacula may continue to develop in succeeding years in sexually mature mink (Mustela vison), the lack of known-age fishers in this series does not make such conclusions possible here. The tentative conclusion reached by de Vos (1952), that bacula were not of value in distinguishing adult from juvenile fishers, resulted from failure to recognize changes 259 80 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 in the rapidly maturing skulls of juvenile male fishers during the late winter. This will be discussed further in a later section. Skulls The specimens were placed in four groups (adult males, juvenile males, adult females, and juvenile females) on the basis of reproductive condition and _ skeletal analysis, and 12 measurements were taken of each skull (see Wright 1953:78-79). Means, standard errors, and coefficients of variation were calculated for each group. It is clear from study of these statistics that the skulls of the juvenile animals in both sexes have not reached maximum growth. In many cases the differences between the means is statistically significant, but, be- cause of overlap between the measure- ments in adults and juveniles, it is not pos- sible to develop aging criteria based on measurement of a single skull parameter, with one exception to be discussed later. The differences between the means of these measurements was generally much greater among males than among females. For example, the mean weight of adult male skulls was 70.6 g, whereas in juvenile males it was 53.9 g, a difference of some 20 percent. In female skulls, however, the adults average 32.1 g and the juveniles 31.1 g, a difference of only 3 percent. The postorbital constriction becomes somewhat smaller with increased age in both sexes of fishers, as it does in other. mustelids. Another striking difference be- MAINE FisHers * Wright and Coulter 81 tween adult and juvenile skulls was seen in males where the zygomatic breadth averages 77.4 mm in adults and only 64.8 mm in juveniles. In spite of this 18 percent smaller measurement in juveniles, there is overlap. It is not possible to classify a male fisher as juvenile or adult solely on the basis of this measurement. The difference in zygomatic breadth would, in most cases, produce a broader appearing face on adult males than on juvenile males. The sutures in the skulls of fishers, like those of all other mustelids, tend to dis- appear at a relatively young age (Marshall 1951:278, Greer 1957:322-323) as com- pared to the Ursidae, for example, where they persist for many years (Rausch 1961: 86, Marks and Erickson 1966:398 ). Juvenile male fishers taken in early fall (Fig. 5A) show almost all of the sutures unfused, but on specimens during March or April (Fig. 5C) almost all have completely disappeared. Eadie and Hamilton (1958:77) showed, in New York fishers from which they had re- productive tracts, that “All breeding fe- males showed at least partial fusion of the temporal ridges . . . to form a sagittal crest, and [that] the maxillary-palatine sutures were completely fused. Non-breeding fe- males showed the temporal ridges in various degrees of separation and had the maxillary- palatine sutures at least partly open. It is concluded that female fisher normally breed at the age of one year in the wild, and that these criteria will separate young- of-the-year from adults.” < Fig. 4. (A) Lateral view of skull of winter juvenile male, February, showing well developed sagittal crest and open zygo- matic—maxillary suture. (B) Lateral view of skull of fully adult male showing typical tremendously developed sagittal crest and disappearance of zygomatic-temporal suture. The heavily worn teeth shown are not necessarily characteristic of adult fishers. (C to J) Bacula of male fishers showing progressive changes with age, distal end to the top, the youngest to the left and oldest to the right. C, D, and E are from juveniles, C taken October 12, D taken December 3, E taken January 5. F and G are from late winter juveniles showing progressive changes toward the adult type with increased deposition of bone at the basal end. Both F and G were taken in February or early March. H, |, and J are selected adult bacula showing the characteristic oblique ridge near the basal end and generally more massive appearance. H is from a smaller-than-average male (body weight, 9 lb, 5 oz), | and J from larger-than-average males (I, carcass weight 10 Ib; J, body weight, 14 Ib 6 02). 261 §2 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 Our findings from study of 66 female fishers from Maine, from which comparable data were available, confirm in detail the findings of Eadie and Hamilton (1958). It is also clear that the maxillary-palatine su- ture is among the last, if not the last, to disappear. These authors also describe a frequency distribution in the length of the sagittal crests in adult females, and reference to their Fig. 3 shows that there are two peaks of sagittal crest lengths which they tenta- tively regarded as representing a group of 1%-year-old females and another group of older females. When we plotted our data in comparable fashion, the line exactly paralleled theirs; and there is thus further evidence that such separation into young adults and older adults is possible. The distribution of the lengths of the sagittal crests of the adult Maine female fishers, plotted in the same fashion as did Eadie and Hamilton, is as follows: 0-10, 1; 11-20, 11; 21-30, 3; 31-40, 8; 41-50, 19; 51-60, 1. The findings in the skulls and skeletons of the two recently bred nulliparous fe- males, whose reproductive tracts were des- cribed in an earlier section, also provide significant evidence that the onset of breed- ing in female fishers occurs when they are 1 year old. In each case there was no sagittal crest, and the maxillary-palatine suture was partially open. Eadie and Ham- ilton (1958:79) found this suture closed in all New York fishers judged to be adults. In their collection, adult fishers, taken en- MaIn_E Fisuers * Wright and Coulter 83 tirely in fall and winter, would have been at least 20 months old, whereas our two animals were almost exactly 1 year of age. One of these animals shows the pubo- ischiac symphysis still open; the other shows it partly closed. Further, the fact that during the fall and winter there is only one type of skull to be found in fishers that have not bred makes it virtually certain that wild Maine fishers are regularly im- pregnated at the age of 1 year and thus produce their first litters at the age of 2 years. The sagittal crests of adult male fishers are extremely well developed as was men- tioned by Coues (1877:65), and the degree of sexual dimorphism in skulls of fishers is greater than in any other American muste- lid. All adult females develop sagittal crests, but even the most highly developed crests in females are almost vestigial com- pared with those of adult males. It is natu- ral to suspect that with this tremendous development in mature males the crest might begin to develop earlier in juvenile males than in females. This is exactly the case, and sagittal crests were first seen in one of two juvenile males taken in Decem- ber (Fig. 5B). By February, March, and April the crests of the juvenile class, now almost 1 year old, are well developed ( Fig. 5C), as much so as they ever become in adult females. In the female fishers it is clear that the sagittal crest develops first at the posterior end of the skull and grows progressively < Figaho- Dorsal view of male fisher skulls showing characteristic changes associated with development. (A) Juvenile male, October 12, showing narrow zygomatic breadth, all sutures in nasal region clearly open; the fronto-parietal sutures are partly fused. The poorly developed temporal lines are wide apart and thus there is no sagittal crest. (B) Juvenile male, December 3, showing disappearance of fronto-parietal suture, less conspicuous sutures in nasal region, and characteristic early development of sagittal crest running throughout the middle and posterior portions of the cranium. (C) Juvenile male in late winter, February, in which these naso-maxillary and maxillary-frontal sutures are barely visible, but the zygomatic-temporal sutures are still very distinct and the sagittal crest is better developed. (Same skull as shown in Fig. 4A). (D) Skull of adult male in which the entire dorsal skull is ankylosed into a single unit; no suture visible except for faint remains of posterior The characteristic highly developed keel-like sagittal crest of all adult males is clearly shown. (Same skull as shown in Fig. 4B). internasal suture. 263 84 = Journal of Wildlife Management, Vol. 31, No. 1, January 1967 forward over a period of months or prob- ably years. In the male fisher the temporal lines move rapidly together during the win- ter months; and as soon as the crest is formed, it runs essentially the entire length of the dorsal region from the postorbital constriction to the inion, a distance of 50- 60 mm. The sagittal crest continues to develop in adult males, and they have the crest developed to the extent of forming a “thin, laminar ridge” (Coues 1877:65). It is difficult to measure the extent of this ridge objectively; but since it extends posteriorly in fully adult males, one can use the method employed by Wright and Rausch (1955) on wolverines to subtract the con- dylobasal length from the greatest length of the skull. This is one accurate method of showing the posterior extension of this crest. This indirect measurement shows no overlap whatever between males classed as adults and those classed as juveniles. The mean for the former group is 11.9 mm and for the latter, 3.9 mm (see Fig. 4, A and B). Thus in male skulls if the differ- ence between the greatest length of the skull and the condylobasal length is 6 or more mm (may be as much as 15 mm), the animal is an adult; if it is less than 6 mm, the animal is a juvenile. Another reason for assuming that skulls of males with immature bacula, but with sagittal crests, are still in their first year of life is provided by data on the closure of sutures in the skull. The last sutures to close in males are the zygomatic-temporal, the naso-maxillary, the internasal, and the naso-frontal. In all of the skulls classed as adult, all of these sutures were closed, but in every male skull classed as juvenile, all four of these sutures were still open (Figs. 4 and 5). On the basis of this evidence, it seems clear to us that males classed by de Vos (1952) as “adults” were in effect juveniles as well as his “juvenile” class, and that only the animals he called “old adults” were adult males over 1 year of age. It is concluded, therefore, that during the early winter, adult males can be sepa- rated from juvenile males by the occur- rence of a well developed sagittal crest on adults; but by mid- or late winter only those males with all of the skull sutures closed are adults. Body Weights Both de Vos (1952) and Hamilton and Cook (1955) have provided body weights of wild-caught fishers, and both studies show that males often weigh twice as much as females. The latter indicate an average weight for males of 3,707 g (8 lb 3 oz) and 2,057 g (4 lb 9 oz) for females. De Vos’s figures are roughly comparable. In both studies many of the body weights were esti- mated from carcass weights by applying a correction factor to skinned carcasses. (Most fisher specimens coming to biologists are likely to be carcasses skinned by trappers. ) Hamilton and Cook (1955:21-22) state that the fresh carcasses average 80 percent of the unskinned weight. In the present study many fishers were confiscated and were available intact. Thus, it was pos- sible to obtain a sample of weights taken directly from the entire unskinned carcasses, allowing consideration of differences be- tween adult and juvenile classes in both Sexes. Data obtained from those fishers which were weighed entire in the laboratory are shown in Table 4. The differences between the juveniles and adults in both sexes is highly significant although there is some overlap in each case. Furthermore, juvenile males are significantly heavier than the adult females. The available mean weights of adults are probably more se*isfactory than those of the juveniles. Presumably, 264 the adults were no longer growing, but the juveniles were growing throughout the collection period from October to April. The sample is not large enough to allow a breakdown within the juvenile classes by month, but the smallest juveniles were taken in the fall. The fact that weights of the juvenile males are 21 percent less than those of the adult males, while the weights of juvenile females are only 15 percent less than those of the adult females, further indicates that juvenile female fishers are more nearly full grown during the first winter of life than are the juvenile males. In many cases, the fishers that were weighed whole were also weighed after skinning. This allowed determination of a correction factor. Thirty-nine animals were weighed both before and after skin- ning: 14 adult males, 5 juvenile males, 8 adult females, and 12 juvenile females. The carcasses averaged 81.9 percent of the whole weight; or, stated conversely, one could multiply the carcass weight by 1.22 to obtain an estimate of the entire adult weight. This latter conversion factor was applied to those animals that were weighed only after being skinned. Esti- mated entire body weights obtained in this fashion were comparable for both adult and juvenile males, but weights of females were significantly below the weights of those females weighed entire. For this reason, it was obvious that in the interval between skinning and weighing, many of the female carcasses had lost significant weight. It was therefore necessary to aban- don any attempt to use the more numerous carcass weights for interpretation of pos- sible growth rates in the juveniles or other weight changes that might exist between months. MaInE FisHers * Wright and Coulter 85 Table 4. Body weights of Maine fishers weighed whole. No. MEAN Bopy SE CLaAss Or WEIGHT IN MAX, MIN. ANI- (OUNCES ) Oz MALS Adult 2 25 Jeet +6.30 14-6 7-4 (10 lb 12 oz) Juv. 2 10 135.5 +7.08 10-8 6-8 (8-714) Adult @ Ie: 88.2 =23.61 (Al) 4578 (5-8) Juv. @ 17 75.0 ORD 6- 8 3-13 (4-11) DISCUSSION This study indicates that in the fisher the adult class consists of all animals more than 1 year of age and that all animals of both sexes less than 1 year are sexually imma- ture. Females older than 1 year normally are carrying unimplanted blastocysts through- out the year except during active preg- nancy in late winter. The fisher, then, differs from all other American mustelids studied in this regard except the wolverine. The weasels, Mustela erminea and M. frenata, are similar in that the males reach sexual maturity in 1 year; but the females breed during their first summer and thus produce young at the age of 1 year (Wright 1963:83-84). In the marten, males also apparently reach sexual maturity in 1 year, but females may not breed until they are 2 years old, and thus two year-classes of immature females may be found in wild populations (Jonkel and Weckwerth 1963: 95-96 ). This has made further refinement of Marshall’s (1951) original study of marten quite difficult. In the female otter it appears that sexual maturity is delayed another year beyond that in the fisher and that there are two age-classes of immature otters (Hamilton and Eadie 1964:245). In the badger the same type of situation prevails as in the fisher except that some females breed pre- cociously during their first summer and 265 86 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 such females would produce litters at the age of 1 year, whereas most badgers pro- duce their first litters at the age of 2 years (Wright 1966:42). Only in the wolverine (Gulo gulo) does it appear that a repro- ductive cycle like that of the fisher is found; but owing to a small sample of ani- mals of the former species, the matter of age at sexual maturity is somewhat in doubt. The recovery of the marten in Maine has been much slower than in the fisher (Coulter 1959) although both species orig- inally occurred sympatrically in much the same habitat. The present study indicates that the potential rate of reproduction in the fisher is higher than in the marten. A large sample of winter-caught marten is not available from Maine, but such material was obtained from Montana. Wright (1963: 79) indicates that corpora lutea counts averaged 3.02 in a sample of 44 trapper- caught marten. The present study showed 3.28 for the fisher. Perhaps of greater sig- nificance, though, is the fact that some female martens (in Glacier National Park) (Jonkel and Weckwerth 1963) do not produce litters for the first time until they are 3 years old. LITERATURE CITED CANIVENC, R., AND M. BONNIN-LAFFARGUE. 1963. Inventory of problems raised by the delayed ova implantation in the European badger (Meles meles L.). Pp. 115-125. In A. C. Enders (Editor), Delayed implantation. Uni- versity of Chicago Press, Chicago, Illinois. 309pp. Coves, E. 1877. Fur-bearing animals: a mono- graph of North American mustelidae. Dept. Interior, Misc. Pub. 8, Washington, D. C. 348pp. Cou.LTer, M. W. 1959. martens in Maine. 152) 50-53. 1960. The status and distribution of fisher in Maine. J. Mammal. 41(1):1-9. DEANESLY, RutH. 1935. The reproductive proc- esses of certain mammals. Part IX: Growth Some recent records of Maine Field Naturalist and reproduction in the stoat (Mustela erminea). Philos. Trans. Roy. Soc. London 225( 528 ):459-492. DE Vos, A. 1952. Ecology and management of fisher and marten in Ontario. Ontario Dept. Lands and Forests Tech. Bull. 90pp. Eapiz, W. R., AND W. J. HaAmitton, Jr. 1958. Reproduction in the fisher in New York. New York Fish and Game J. 5(1):77-83. Exper, W. H. 1951. The baculum as an age criterion in mink. J. Mammal. 32(1):43-50. Enpers, R. K., AND O. P. PEARSON. 1943. The blastocyst of the fisher. Anat. Rec. 85(3): 285-287. Greer, K. R. 1957. Some osteological charac- ters of known-age ranch minks. J. Mammal. 38(3):319-330. Hatt, E. R. 1942. Gestation period in the fisher with recommendations for the animal’s pro- tection in California. California Fish and Game 28(3):143-147. HamixTon, W. J., Jz., AND A. H. Coox. 1955. The biology and management of the fisher in New York. New York Fish and Game J. 2(1):13—35. , AND W. R. Eapie. 1964. Reproduction in the otter (Lutra canadensis). J. Mammal. 45(2):242-252. JONKEL, C. J., AND R. P. WeEcKWERTH. 1963. Sexual maturity and implantation of blasto- cysts in the wild pine marten. J. Wildl. Mgmt. 27(1):93-98. Marks, S. A., AND A. W. ERICKSON. determination in the black bear. Memt. 30(2):389-410. MarsHati, W. H. 1951. An age determination method for the pine marten. J. Wildl. Mgmt. 15(3) :276-283. NEAL, E. G., AND R. J. Harrison. 1958. Re- production in the European badger (Meles 1966. Age J. Wildl. meles L.). Trans. Zool. Soc. London 29(2): 67-130. Rauscu, R. L. 1961. Notes on the black bear, Ursus americanus Pallas, in Alaska, with par- ticular reference to dentition and growth. Z. Saugetier. 26(2):77-107. Rurrie, A., M. BONNIN-LAFFARGUE, AND R. CaniveNc. 1961. Les taux du pregnandiol urinaire au cours de la grossesse chez le Blaireau europeen. Meles meles L. Comptes rendus des séances de la Société de Biologie 155(4):759-761. Taper, R. D. 1956. Characteristics of the pelvic girdle in relation to sex in black-tailed and white-tailed deer. California Fish and Game 42(1):15-21. 266 MaINE Fisners « Wright and Coulter 87 WricuT, P. L. 1948. Preimplantation stages in University of Chicago Press, Chicago, Illinois. the long-tailed weasel (Mustela frenata). 309pp. Anat. Rec. 100(4):593-607. 1966. Observations on the reproductive 1950. Development of the baculum of cycle of the American badger (Taxidea taxus). the long-tailed weasel. Proc. Soc. Expt. Biol. Pp. 27-45. In I. W. Rowlands, Editor, Com- and Med. 75:820-822. parative biology of reproduction in mammals. 1953. Intergradation between Martes Symposia Zool. Soc. London, No. 15. Aca- americana and Martes caurina in western demic Press, London. 527pp. Montana. J. Mammal. 34(1):74-86. , AND R. Rauscu. 1955. Reproduction in 1963. Variations in reproductive cycles the wolverine, Gulo gulo. J. Mammal. 36(3): in North American mustelids. Pp. 77-97. In 346-355. A. C. Enders (Editor), Delayed implantation. Received for publication August 22, 1966. 267 BIOLOGY OF REPRODUCTION 4, 239-247 (1971) Ecological Adaptation and Mammalian Reproduction C,H. CONAWAY Caribbean Primate Research Center, University of Puerto Rico, San Juan, Puerto Rico 00905 Received September 9, 1970 In this paper some of the major variations in mammalian reproductive cycles are dis- cussed from the viewpoint of their broad adaptive values. The variations involve quali- tative differences in various aspects of the reproductive cycle and seem to be genetically fixed within a species. Research in the area of reproductive physiology has chiefly been confined to a few laboratory and domestic species which have been studied in great detail. As a result we have much information about these few forms, but perspectives may be distorted by this same wealth of informa- tion. It is often forgotten that these studies have been made on highly specialized forms which are usually the resultant of many years of domestication and artificial selection. Furthermore, the work has been done with- out regard to ecological or social context. For example, so much emphasis has been given to studies of the nonpregnant cycle, that we tend to lose insight into its signifi- cance in natural populations. In natural populations the nonpregnant cycle is a rarity, and it is essentially a patho- logical luxury which cannot be tolerated. Even in relatively long-lived animais with low mortality rates a nonpregnant cycle 1s an exception. In a study done under the somewhat artificial conditions existing in the Cayo Santiago Island colony in Puerto Rico, only 6 of the 28 fertile mature female rhesus monkeys (Macaca mulatta) in a free ranging social group failed to conceive on the first estrus of the breeding season (Conaway and Koford, i964). The remaining six conceived during their second estrous period. For short-lived prey species the occurrence Copyright © 197i by The Society for the Study of Reproduction of a nonpregnant cycle is a disaster, which must be avoided if the individual is to con- tribute significant numbers of offspring to the population. Many small mammals in this category have only a few months of repro- ductive life. Any portion of this which is lost through a nonpregnant cycle can be critical. The only acceptable alternatives are either to safeguard against the occurrence of a non- pregnant cycle or to recover and recycle as quickly as possible. One of the basic variants in mammalian reproductive cycles seems to be in the methods which have evolved for handling the nonpregnant cycle or preventing its occurrence. Full understanding of these variations is impossible since we have de- tailed information about the nonpregnant cycle in fewer than 50 of the 1000 mam- malian genera. This is not surprising since information must come from laboratory studies; however, it does indicate the impor- tance of obtaining basic information on a wide variety of forms. CLASSIFICATION OF BASIC TYPES OF NONPREGNANT FEMALE REPRODUCTIVE CYCLES Everett (1961) clearly defined pseudopreg- nancy and indicated sources of confusion in the usage of this term. As he proposed, the term pseudopregnancy will be used here to indicate the occurrence of any functional luteal phase in a nonpregnant cycle. The pseudopregnancy wil) be designated us “Spontaneous” if the formation of a func- tional corpus luteum always follows ovula- tion. If activation of the corpus luteum does not obligatorily follow ovulation but re- 239 268 240 quires a separate stimulation as in the labora- tory mouse and rat, the phenomenon will be designated as “induced pseudopregnancy.” Within this framework mammalian female cycles may be broadly categorized as follows: Type I Both ovulation and pseudopregnancy are spontaneous. Sterile copulation does not alter the length of the progestational phase. Subtype A. Medium length cycles (gener- ally 2-5 weeks long). The follicular phase is somewhat variable and may last from a few days to several weeks. This variation accounts for the major difference in lengths of cycles between species in this group. The luteal phase is relatively constant, lasting about 12-16 days. Cycles of this type appear to be the rule in ungulates, hystricomorph, rodents, and higher primates. Subtype B. Long cycles (over 5 weeks in length). The follicular phase is several weeks in length and the luteal phase is prolonged, lasting from 1 to 2 months. A period of anestrus follows the luteal phase. Cycles of this type occur in the dog and probably other canids. Type II Ovulation is induced; pseudopregnancy is spontaneous. When ovulation is induced by exogenous hormones, the length of the luteal phase does not differ from that following sterile copulation. Subtype A. Medium length cycles (less than a month in length). Estrus is more or less behaviorally induced by proximity to the male or by social stimulation. The length of estrus may be extended in some species by continued behavioral stimulation. Synchro- nization of estrus in all members of a popu- lation through social facilitation occurs fre- quently. Cycles of this type seem character- istic of the Microtini, Lagomorpha, and some insectivores including the Soricidae. A typical example of this type of cycle is shown by the cottontail rabbit (Sy/vilagus CONAWAY floridanus). In most areas the cottontail is a seasonal breeder with the breeding season Starting during the spring and ceasing in late summer. The gestation period is 27 days and each female breeds during the postpartum estrus within 0.5 hr following parturition (Marsden and Conaway, 1963). During the breeding season a total of five to seven litters may be produced. Within any single popula- tion the time of onset of the breeding season may vary considerably between years; how- ever, most of the females in that population usually conceive within a brief period each year and the population may remain in very close synchrony throughout the breeding season. Synchronization of estrus seems to be the result of behavioral displays which influence all members of the population. The importance of behavioral induction of estrus is Shown to an even greater degree in the similar cycle cf the prairie meadow vole (Microtus ochrogaster). The onset and dura- tion of estrus are largely dependent upon social stimulation. Proximity to the male is the most potent estrus-inducing stimulus, although various social and environmental stimuli are also somewhat effective. If stimu- lation iS continuous, a state of constant estrus can be maintained for at least 30 days. Copulation at any time during estrus results in ovulation 10.5 hr later (Richmond and Conaway, 1969). Subtype B. Long cycles (4-8 weeks in length). Estrus is more spontaneous and its duration is more fixed than in Subtype A. The luteal phase of the nonpregnant cycle persists from 4 to 6 weeks. This type of cycle is known to occur in the domestic cat and ferret, Type IIT Both ovulation and corpus luteum forma- tion are spontaneous, but pseudopregnancy is induced via the release of luteotropin following copulation. In the short cycle (noncopulatory), no functional corpora lutea form and ovulation recurs after 4-7 days. 269 ECOLOGICAL ADAPTATION AND REPRODUCTION If sterile copulation occurs the resulting pseudopregnancy is similar to that of me- dium length cycles (Types I A and II A). This highly specialized cycle is known to occur in several groups within two rodent families, the Cricetidae and the Muridae. If one examines the preceding types of female reproductive cycles with regard to ecological adaptation, several speculations seem warranted. Many small mammals, in- cluding many rodents, insectivores, and lago- morphs, may be characterized as staple small prey species. They have very short life-spans, often in the vicinity of 3-5 months. Mortality rates are extreme and annual production by an adult female which survives the repro- ductive season is very high (30-35 young per adult female per breeding season in cotton- tails). Sexual maturity occurs very early, usually at 1-2 months of age. High produc- tion rates are essential to the survival of the species and such animais cannot afford to be nonpregnant during the breeding season. Two different systems of safeguards appear to have been developed to minimize non- pregnant time. One of these is the Type II A cycle using induced ovulation and the second is the Type III cycle involving induced pseudopregnancy. In either case there is no protection against sterile copulation, since there is a pseudopregnancy of approximately 2 weeks. Sterile copulation, however, seems virtually unknown in natural populations. Despite the fact that it has been so in- tensively studied and is so familiar, the Type III cycle seems to be of very restricted occurrence among mammalian species. It has been identified in a few members of each of two very large rodent families, the Cri- cetidae and the Muridae. These families have been separated for a considerable period of time and have shown some parallel evolution with the development of numerous ecologi- cally equivalent species. The family Muridae, commonly called the Old World rats and mice, consists of 101 genera distributed in seven or eight sub- 241 families. Within this assemblage, five species of Rattus and one of Mus clearly have been shown to have the Type III cycle. All of these are typical high production, small prey species. On the other hand, the large pseudo- myid murid Mesembriomys of Australia has a Type I A cycle. The mean length of the nonpregnant cycle in this species is 26 days. Ovulation is spontaneous followed by spon- taneous pseudopregnancy lasting about 14 days (Crichton, 1969). Indirect evidence suggests that the Type I A cycle also occurs in other pseudomyid and perhaps hydromyid murids, although none of these forms can be considered as a high reproductive rate small prey species. All seem to have only a few litters per year and very few young per litter. They differentiated during the Miocene in the absence of pla- cental carnivores (Simpson, 1961) and thus are not adapted to high levels of predation pressure. Within the genus Rattus there are several ecologically similar forest-dwelling species which have very low reproductive rates (Harrison, 1952) and apparently low mortality rates. It would be very useful to learn about the cycle of, these forms which are closely related to the familiar Rattus species having the Type III cycle but eco- logically very different and occupying a niche similar to that of Mesembriomys. The Cricetidae is the second family of rodents in which the Type III cycle occurs. This family contains 99 genera divided among five subfamilies. The largest of these is the Cricetinae with 59 genera. In this sub- family at least six genera appear to have one or more species showing the Type II cycle. Also at least 2 of the 13 genera of the sub- family Gerbillinae appear to have this cycle. Several species of the genus Microtus in the subfamily Microtine, however, are known to have typical Type If A cycle. One might predict that still a third type of cycle might occur in this family since the Malagasy rats (subfamily Nesomyinae) are in many ways 270 ecologically similar to the Australian rats and therefore may have Type I A cycle. Both the Type II A and Type III cycles seem to be characteristic of short life-span, high production prey species. Probably both types have developed idependently in several groups. The Type II A cycle is found in at least three orders, while the Type III cycle is known from some groups in only two highly specialized rodent families. The special adap- tive significance of the Type HI cycle is not clear. One possible suggestion is that those forms having the Type III cycle do not show the violent amplitude in population density cycles that characterize many Type II A forms. It is possible that since there is less estrous induction by behavioral stimulation in Type III spontaneous ovulators, the major reproductive outbursts and subsequent den- sity-dependent die-offs are to some extent dampened in the Type III cycle. Many Type II A forms such as voles and hares are characterized by major cyclic fluctuations in population density. If the short cycle (Type III) and medium length cycle with induced ovulation (Type I] A ) are associated with high turnover prey species, what can be said of the other cycle types? It seems that medium length cycles with spontaneous ovulation (Type I A) in- clude in general the medium and larger herbivores, such as ungulates, hystricomorph rodents, and the omnivorous primates. These are long-lived prey species not subjected to the extreme mortality rates of smaller forms. Recovery from a nonpregnant cycle would be important but extreme rapidity would not be critical. Therefore these animals can afford a delay of several weeks before re- cycling. The long cycle Types I B and II B seem restricted to large predators in which the emphasis may be on low production rather than high production. The question now arises: which is the primitive Eutherian pattern—the medium length or the long cycle? Is this the basic birth control mecha- CONAWAY nism, or have other forms been forced to shorten a long cycle to increase production? One can only speculate about this at present, since information from so many groups is completely lacking. One point which may apply is that in the primitive insectivore family Tenricidae, the length of pseudopregnancy seems prolonged and the cycle appears to be Type JI B (C. H. Conaway and M. J. Hasler, unpublished). In the more advanced Soricids, however, the cycle is of the II A type (G. L. Dryden and C. H. Conaway, unpublished). These data would support the concept that long luteal life was the primitive pattern. On the other hand, the two major insectivore subgroups had already diverged by the middle Creta- ceous (McKenna, 1969). Tenrecs and Carniv- ora were derived from palaeoryctoid In- sectivora while the shrews and most other Cutherian mammalian orders trace to a leptictid-like insectivore stock. It may thus be that the medium-lived and the long-lived corpus luteum forms represent early and fundamental divergences not related to their present ecological adaptations. INDUCED AND SPONTANEOUS OVULATION As information is obtained about more forms it appears that induced ovulation is the more widespread phenomenon and that spontaneous ovulation occurs in a more re- stricted number of species. Since most of the common domestic and laboratory species are spontaneous ovulators, this point is often overlooked. It has also become increasingly apparent that, physiologically, both induced and spontaneous ovulation are the extremes of a single continuum. Some induced ovula- tors will ovulate under a variety of stimuli other than copulation. It is a common ob- servation that the domestic rabbit will ovu- late as a result of female-female mounting, as well as other stimuli. On the other hand, in spontaneous ovulators there is a copula- tory LH surge similar to that found in in- 271 ECOLOGICAL ADAPTATION AND REPRODUCTION duced ovulators (Taleisnik, Caligaris, and Astrada, 1966). Induced ovulation appears to be of gen- eral occurrence in the primitive Eutherian order of Insectivora. Within the Rodenta, it occurs in some of the primitive Sciuro- morpha while most of the more advanced Hystricomorpha seem to be spontaneous ovulators (Asdell, 1964). Also as previously noted, induced ovulation is of very wide- spread occurrence. Because of these reasons, it seems that induced ovulation may be re- garded as the basic Eutherian pattern and spontaneous ovulation as a specialization. Other than Type III rodents, spontaneous ovulation occurs generally in ungulates (ex- cept Camelidae), primates, canid carnivores, and in hystricomorph rodents. It is sporadi- cally distributed in other groups (Asdell, 1966). Asdell (1966) concluded that because of the sporadic nature of the distribution of the two types of ovulation, no conclusion could be drawn regarding evolutionary trends of this character. For the ungulates, primates, and canids, at least, one can propose a common selective force favoring the develop- ment of spontaneous ovulation. All of these forms are characterized by having fairly complex social groups with often elaborate social structuring. Temporary pair bonding and consort relationships are common be- tween an estrus female and a breeding male and the number of adult females usually exceeds the number of breeding males. Commonly breeding activity is restricted to a small segment of the adult male population which includes only animals of high social rank. In a situation where the number of effec- tive breeding males may be considerably less than the number of breeding females, it would be of great advantage to spread the estrous periods of females randomly over a period of time to insure conception in all females. Since induced ovulation seems to be accompanied by more or less synchroniza- 243 tion of estrus periods, a strong positive selective force favoring spontaneous ovula- tion and randomization of estrus periods would exist when the number of breeding males was limited. The female which could achieve estrus independently and avoid estrus synchronization would have a greater chance of conception. This explanation, however, does not seem to fit all of the histricomorph rodents. While some of these species (viscacha and chin- chillas) are colonial and may have a reduced number of breeding males, certainly others such as the porcupine are solitary. The occurrence of induced ovulation in the alpaca, llama, and probably other Camelidae (England et al., 1969; Fernandez-Baca, Madden, and Novoa, 1970) also would not be explained by this hypothesis. Also some degree of estrus synchroniza- tion may occur in spontaneous ovulators. The Whitten effect may involve estrus syn- chronization (Whitten, 1956), but the im- portance of this in natural populations re- mains to be demonstrated. Kummer (1968) found that among hamadryas baboons in one male units having two adult females there was a high degree of estrous synchro- nization between the two females. Larger units, however, showed less suggestion of synchronization. An extreme degree of es- trus synchronization has been reported for Lemur catta where observed mating lasted only 1 week in a troop containing nine adult female lemurs (Jolly, 1966). In bands of rhesus monkeys there is no evidence of es- trous synchronization among the individual females (Conaway and Koford, 1964); how- ever, there is some suggestion that the peaks of mating activity may vary between troops (Koford, 1965). DELAYED IMPLANTATION Delayed implantation has clearly arisen independently a number of times. Not only does it occur in widely scattered species and groups within many orders but also the 272 244 physiological controls vary. The selective forces favoring delayed implantation seem clear in most forms. The fundamental pre- requisite is that the young be born at the optimum season of the year for survival and growth. In addition, within each species the length of the implanted gestation period is relatively rigidly fixed. Only heterothermic bats seem able to alter this significantly through delayed development (Bradshaw, 1962; Racey, 1969). Within these funda- mental restrictions problems arise under several conditions. In boreal areas solitary mammals may have difficulty in crowding mating, gestation, birth and rearing of the young to independ- ency within the short growing season. A solution to this problem is in delayed im- plantation which allows almost complete flexibility of the time interval between mating and birth. Delayed implantation in northern mustelids, ursids, and roe deer would seem to fit this pattern. The same forces apply when the time for mating, birth, and rearing of the young is behaviorally restricted to a brief period each year. Again all the reproductive events must be crowded into a short time interval. This is the problem faced by the colonial seals. The sexes are together for only a short period of time each year and must breed, give birth, and rear young during this interval. Delayed implantation in marsupials seems to serve an entirely different function. Those forms showing the delayed implantation live in a severe and unpredictable environment. There is a prolonged nursing period during which the suckling young may frequently be lost as a result of severe environmental con- ditions. If this occurs, the loss of suckling stimulus causes an unimplanted blastocyst to break diapause and begin development. In this case implantation serves as a means to replace the lost suckling young as quickly as possible so that advantage can be taken of any improvement in environmental condi- tions. CONAWAY At present I can offer no explanation of delayed implantation in New World Eden- tata or in the African bat Eidolon. Perhaps when more is learned about the natural history and ecology of these forms the sig- nificance of delayed implantation to them will become apparent. SEASONAL BREEDING It is becoming increasingly clear that at least some degree of seasonality in repro- ductive activity is almost universal in natural populations. This is true not only in the boreal and temperate zones but also in the tropics. Among natural populations one of the carefully documented studies which suggest continuous breeding is that done on the musk shrew (Suncus murinus) on Guam (Dryden, 1969). The breeding season may not be regular, however, nor is it necessarily limited to one period each year. Desert species are often opportunistic breeders and breed irregularly following rainfall. In small rodents in the temperate zone there may be two distinct breeding seasons within the year. Several species of Peromyscus have a spring and fall breeding season with midsummer and mid- winter cessations of reproduction (Hull, 1966). Generally, seasonality quickly and more or less completely disappears when species are brought into the laboratory. This is evident with small mammals. Many studies have been directed toward a search for the environmental trigger which initiates reproductive activity. For many small mammals having short gestation peri- ods it seems that a reverse approach may be more ecologically and physiologically sound. If these forms are regarded as potentially continuous breeders then the problem is to understand the environmental factor or combination of factors which depresses re- production. Among such factors extreme de- viations of temperature and aridity are certainly important. Extremely short photo- 273 ECOLOGICAL ADAPTATION AND REPRODUCTION period may have a depressing effect in some species, and lowered quality of nutrition is probably also effective. In a 3-year study in the Congo involving over 7000 specimens of several species, Dieterlen (1967) found both species and annual variations in the breeding seasons. He concluded that in general, the annual amplitude of reproductive periodicity was proportional to the degree of seasonal contacts. Small mammals seem to be able to adapt to reproduce under almost any set of environmental conditions, but deviation from these conditions inhibits reproduction. If the viewpoint outlined above is adopted, then many variations in the reproductive season seen in natural populations can be explained. Instances of “‘unseasonal”’ early breeding in cottontail rabbits during a period of warm weather in midwinter (Hill, 1966) or extension of the breeding season and occas- sional continuous breeding throughout the winter in small rodents (Ashby, 1967; Krebs, 1964) could both be interpreted as indicating that those species were continuous breeders unless inhibited by adverse environmental conditions. Similarly the spring and _ fall breeding seasons of Peromyscus (Brown, 1964) would fit such a pattern. Voles have been found to continue to breed in irrigated fields after breeding had ceased in voles living in nearby nonirrigated areas (Bodenheimer, 1949). Again this seems to be best explained if one considers them as fundamentally con- tinuous breeders but recognizes that repro- duction may be inhibited by any of a variety of adverse factors. In a regularly fluctuating environment, forms with longer gestation need to predict the optimum season for birth. Here it be- comes imperative to use some regular and repeating event in the environment as a trigger for the breeding season. As has been Suggested many times, variation in photo- period is the most predictable changing factor in the environment and seems to be the clue used by a number of ungulates with six- to nine-month gestation periods. 245 POSTPARTUM ESTRUS Postpartum estrus seems to have devel- oped independently many times and its dis- tribution is sporadic throughout many mam- malian species. As Asdell (1964) has noted, it does not follow any phylogenetic pattern. Indeed it may not occur in all species of the same genus, as in Peromyscus (Asdell, 1964). Apparently the acquisition or loss of a post- partum estrus is one of the most easily made of the major reproductive adjustments. It can be a mechanism for increasing productivity and this seems its obvious function in short life-span, small mammals. It seems almost universal in those forms having Type II A or Type III cycles, while among Type I A forms it is common in the Hystricomorpha. Among other forms it 1s also known to occur in the mouse-sized pygmy squirrel (Exilisciurus exilis) of Malaysia (Conaway, 1968). This seems to emphasize the adaptive role of the postpartum estrus since it has not been re- ported from other squirrels or in fact from any other families of sciuromorph rodents. It also would be expected to occur in several species of Perognathus such as P. parvus and in other Heteromyinae which are typical small prey species, and in this respect similar to the pygmy squirrel. A second group in which the postpartum heat has developed is the colonial seals. As discussed previously, in these forms the sexes are together for only a short period of time into which all reproductive events must be crowded. The postpartum estrus is integrated with delayed implantation. In marsupials also the postpartum heat is associated with delayed implantation and functions with it as an adaptation to an unpredictable environ- ment as previously discussed. DISCUSSION This discussion has considered the major reproductive patterns which are relatively fixed within a species and change slowly over many generations. Another significant group 274 246 of adaptive changes is the flexible quantita- tive changes that vary frequently within a Species or even within an individual. These include variations in litter size, resorption Tate, age at Sexual maturity, number of litters, etc. These are the finer adjustments to specific environmental fluctuations and may be influenced by a wide variety of physical and behavioral variables. An excellent dis- cussion of these has been given recently by Sadleir (1969). Many of the speculations made in this paper may be erroneous. Jt does seem neces- sary to begin to try to understand the signifi- cance of the variations seen in reproductive cycles. Otherwise they become a meaningless and endless array. It also seems that after trying to establish some basic patterns we can then select appropriate species to test some of the hypotheses rather than hap- hazardly studying forms just because they are available and no one has worked with them. It would seem much more useful to study in detail one of the forest rats of the genus Rattus such as R. sabanus than to con- tinue studying species of Rattus which are ecologically similar to the Norway rat. This might provide some evidence regarding the relative importance of adaptation versus phylogeny in establishing basic reproductive patterns. REFERENCES ASDELL, S. A. (1964). ‘Patterns of Mammalian Reproduction.’’ Cornell Univ. Press, Ithaca, N. Y. ASDELL, S. A. (1966). Evolutionary trends in physiol- ogy of reproduction. Jn ‘‘Comparative Biology of Reproduction in Mammals” (I. W. Rowlands, ed.), pp. 1-13. Academic Press, New York/London. AsuBy, K. R. (1967). Studies on the ecology of field mice and voles (Apodemus sylvaticus, Clethrionomys glareolus, and Microtus agrestis) in Houghall Wood, Durham. J/. Zool. 152, 389-513. BODENHEIMER, F. S. (1949). Problems of vole popula- tions in the Middle East: Report on the population dynamics of the Levant vole (Microtus guentheri). Res. Counc. Isr. 77pp. BRADSHAW, G. V. R. (1962). Reproductive cycle of the California leafnosed bat Macrotus californicus. Science 136, 645-6. CONAWAY Brown, L. N. (1964). Reproduction of the brush mouse and white-footed mouse in the central United States. Amer. Midl. Natur. 72, 226-240. Conaway, C. H. (1968). Postpartum estrus in a sciurid. J. Mammal. 49, 158-159. Conaway, C. H., AND Kororb, C. (1964). Estrous cycles and mating behavior in a free ranging band of rhesus monkeys. J. Mammal. 45, 577-588. CRICHTON, E. G. (1969). Reproduction in the Pseu- domyine rodent Mesembriomys gouldii. Aust. J. Zool, 17, 785-797. DIETERLEN, F. (1967). Jahreszeiten und Fortpflanzungs Perioden bei den Muriden des Kivuss-Gebietes (Congo). Z. Saug. 32, 1-44. Drypden, G. L. (1969). Reproduction in Suncus murinus. In “Biology of Reproduction in Mam- mals.” pp. 377-396. Blackwell, Oxford. ENGLAND, B. G., Foote, W. C., MATTHEWS, D. H., Carpozo, A. G., and Riera, S. (1969). Ovulation and corpus luteum function in the llama (Lama glama). J. Endocrinol. 45, 505-513. Everett, J. W. (1961). The mammalian female reproductive cycle and its controlling mechanisms. In “Sex and Internal Secretions” (W. C. Young, ed.), 3rd Ed., Vol. II, pp. 497-555. Williams and Wilkins, Baltimore. FERNANDEZ-BACA, S., MADDEN, D. H. L., AND Novoa, C. (1970). Effect of different mating stimuli on induction of ovulation in the alpaca. J. Reprod. Fert. 22, 261-267. Harrison, J. L. (1952). Breeding rhythms of Selangor rodents. Bull. Raffles Mus. 24, 109-31. Hix, E. P. (1966). Some effects of weather on cotton- tail reproduction in Alabama. Proc. Annu. Conf. Southeastern Ass. Game Fish Commissioners, 19, 48- ayk Jotty, A. (1966). “Lemur Behavior.’’ Chicago Press, Chicago. Kororp, C. B. (1965). Population dynamics of rhesus monkeys on Cayo Santiago. Jn ‘Primate Behavior” (I. DeVore, ed.), pp. 160-174. Holt, Rinehart, and Winston, New York. Kreps, C. J. (1964). The lemming cycle at Baker Lake, Northwest Territories, during 1959-62. Artic Inst. N. Amer. Tech. Paper No. 15, 1-104. Kummer, H. (1968). “Social Organization of Hama- dryas Baboons.”’ Univ. of Chicago Press, Chicago. MarsDENn, H., AND Conaway, C. H. (1963). Behavior and the reproductive cycle in the cottontail. J. Wildl. Manage. 27, 161-170. McKenna, M. F. (1969). The origin and early differentiation of Eutherian mammals. J ‘“‘Com- parative and Evolutionary Aspects of the Vertebrate Central Nervous System,” pp. 217-240. New York Academy of Science, New York. Racey, P. A. (1969). Diagnosis of pregnancy and experimental extension of gestation in the pipistrelle Univ. of 275 ECOLOGICAL ADAPTATION AND REPRODUCTION bat, Pipistrellus pipistrellus. J. Reprod. Fert. 19, 465-474. RICHMOND, M., AND Conaway, C. H. (1969). In- duced ovulation and oestrus in Microtus ochrogaster. In “Biology of Reproduction in Mammals,” pp. 357-376. Blackwell, Oxford. SADLEIR, R. M. F. S. (1969). “The Ecology of Repro- duction in Wild and Domestic Mammals.” Me- thuen, London. 247 Simpson, G. E. (1961). Historical zoogeography of Australian mammals. Evolution, 15, 431-446. TALEISNIK, S., CALIGARIS, L., AND AsTRADA, J. J. (1966). Effect of copulation on the release of pituitary gonadotropins in male and female rats. Endocrinology 79, 49-56. Whitten, W. K. (1956). Modification of the oestrus cycle of the mouse by external stimuli associated with the male. J. Endocrinol. 13, 399-408. 276 Early Growth, Development, and Behavior of the Richardson Ground Squirrel (Spermophilus richardsoni elegans) TIM W. CLARK2 Department of Zoology and Physiology, University of Wyoming, Laramie 82070 AsstrAct: Data on growth and development were collected from five litters (30 individuals) of Richardson ground squirrels (Spermophilus richardsoni elegans) born in captivity. Hair first appeared on the head at 10 days of age and fully covered the body by day 25. Incisors erupted at 13-14 (lower) and 22-26 (upper) days of age. On day 14 trills were first noted. Eyes opened 21-24 days and ears opened 21-26 days after birth. Young were weaned at 28-35 days. Body weight increased at an instantaneous growth rate of 11.4% per day during the first weeks after birth and 2.0% at 10 weeks; 25% of body weight growth was completed by day 35, 50% by day 49, 75% by day 60 and 100% by day 100. Of the linear measurements foot length achieved adult size first (100% in 42 days), tail length next (100% in 56 days) and total length last (100% in 63 days). INTRODUCTION Twenty-eight species of ground squirrels (Spermophilus spp.) are currently recognized (Hall and Kelson, 1959). A review of the liter- ature revealed early growth and development information on only 10 species. The existing data are not complete in all cases and much of the information was gathered in conjunction with studies on other phases of their biology. The purpose of this paper is to describe the early growth, develop- ment, and behavior of the Richardson ground squirrel (S. richardsoni elegans) in southeastern Wyoming. METHODS AND MaTERIALS Litters used in this study were obtained from live-captured preg- nant females taken in April 1968 in the short grass prairie south of Laramie, Albany Co., Wyoming. (Squirrels were kept in individual, wire mesh cages (ca. 56 X 51 X 38 cm.) A wooden nest box (ca. 20 X 20 X 20 cm) with a5 X 5 cm hole cut in one side near the top was placed in each cage. Surgical cotton was used for the nest material. Unlimited amounts of a mixture of whole wheat, corn, alfalfa pellets, lettuce, cabbage, carrots, fresh green grass, small amounts of deer meet, and Purina dog chow were provided. Data on growth and development were collected from five litters — a total of 30 individuals. The young were weighed and measured indi- vidually at various intervals. Individuals were carefully removed from the nest box and replaced after data collection. Since information is 1 Present address: Department of Biology, Wisconsin State University, Med- ford Branch Campus, Medford 54451. 197 / 277 198 THE AMERICAN MIDLAND NATURALIST 83(1) available on the weight of newly born Richardson ground squirrels (Denniston, 1957), and in an attempt to reduce the possibility of ma- ternal cannibalism, it was decided not to measure and weigh all the young during the first two weeks. At 14 days after birth and at each 7- day interval thereafter, the young of all litters were weighed and mea- sured. Young were toe-clipped for individual identification when two weeks old. The following measurements were taken (in mm) for all the pups, body length, tail length, and right hind foot and body weight in g. Total length was obtained by adding the tail length to the body length. Percentage of adult size attained by S. richardsoni young was based on measurements of a series of adults of both sexes collected in the Laramie Basin of southeastern Wyoming throughout the seasonal activ- ity cycle. Maximum (100%) of adult size was taken as the mean of the measurements recorded from 50 animals. A system proposed by Brody (1945) to analyze measurements was used. Measurement values were plotted on a logarithmic scale, versus age on an arithmetic scale. On this plot, linear segments indicate periods when growth increments were a constant percentage of pre- vious size. From these linear sections instantaneous growth rates were calculated from the formula: IGR = (InM, -1InM,) / (t:—-t:) where IGR is the instantaneous percentage growth rate for the unit of time in which t, and t, are expressed and InM, and InM, are the natural logarithms of the measurements made at t, and tp. RESULTS PHYSICAL DEVELOPMENT AND BEHAVIOR At two days after birth Richardson ground squirrels are reddish in color. Some blood vessels are visible beneath the relatively smooth and translucent skin. The internal organs are faintly visible in some pups. The pinnae are evidenced only by slight irregularities in the skin. Small vibrissae are present on the snout, the longest of the series ex- tending posteriorly to about the anterior margin of the eye. The fused digits lack pigmentation. The tail is short and tapering. Audible squeaks are emitted. The pups can be sexed at this time, roll about quite actively with no special orientation, and cannot crawl or right themselves when placed on their backs. By day 5 most pups have lost the stump of their umbilical cords. The toes are still fused, but the claws are fully separated and colored gray at the bases. The dorsal and lateral areas of the head and body are covered with gray pigment. The underparts are still pinkish. The eye region is very darkly pigmented. Pups are eliminating yellow feces at this time. They are barely able to pull themselves forward with their forelegs. Pups are able to right themselves with much apparent difficulty when placed on their backs, 278 EARLY GROWTH OF GROUND SQUIRREL CLARK 1970 See M OT br-66 I9T +9 1D OiGd LLE+8L9 GOS-09G Lol +6 €8¢ 666" “OSG EEE ILE GG bb-66 I6TFE TP 91-69 LLY+GL9 G6c-0G¢ C8 IT+PV Ile ‘68c- “661 1490648 0b2 CG SREY (65 Eh-6E 8h c+Ll OF 92-09 PLO+ELI C86-CbG C8 TIL+S° F9¢ “9Gc- “6FT 19°CE +8004 GC SYS9M 8 Eh-6e SU T+L0P VL-8S FIVG+h 49 896-EE¢ Pr IT+00G¢ ‘80c- “dcl Te'8c+T 991 CG NY Bar! 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By day 8 all claws are completely pigmented. At 11 days the lower incisors are visible just below the surface of the gums. They perforate the gum on day 12, and are well above the gum line on days 13 and 14. At two weeks, the hair at the base of the nose has the characteristic rust-reddish adult color. The tail is covered with very short fine hairs, as is the body. The toes are fully separated and the pups can easily pull themselves forward with their forelegs. When placed on their backs they readily right themselves. The young utter a half-muted trill when disturbed. At three weeks the upper incisors begin to appear through the gum line and by day 26 have erupted. The eyes of some pups are open on day 21 and by day 24 all young have their eyes open. Both eyes do not always open at the same time. The external auditory meatus is open by day 26. Young frequently leave the nest box shortly after the eyes open. The pups are not as vocal as before. They do not evert their anal glands or “bottle brush” (Bridgewater, 1966) when handled as is characteristic of adults. At four weeks the young have acquired adult coloration. They WEIGHT IN GRAMS AGE IN DAYS Fig. 1—Growth in weight of young Spermophilus richardsoni elegans raised in captivity. Value above segments of curve are instantaneous growth rates. The value times 100 equals the percentage of increase per day during a par- ticular age period. 280 1970 Crark: EARLY GROWTH OF GROUND SQUIRREL 201 run well and do not wobble while running. Pups urinate when handled and exhibit some resistance. A few pups can evert their anal gland and some attempt to bite. Solid brown feces are beginning to appear. At five weeks the young are passing dark fecal pellets, apparently indicating a change from milk to a solid diet at the time of weaning (Neal, 1965). Tail-flicking was first noticed at this time. INCREASE IN BODY WEIGHT Weight (g) and measurements (mm) of young Richardson ground squirrels from birth through 10 weeks of age are given in Table 1. The mean weight at two days of age of Richardson ground squirrels was 5.9 g (sp = + 1.5), with a range of 5.5 to 6.6 g. Weight of one-day-old Richardson ground squirrels as reported by Denniston (1957) averaged 5.96 g and for other Spermophilus from birth to one day old are: S. spilosoma, 3.8 g (Sumrell, 1949) ; S$. tridecemlineatus, 2.6 ¢ (Wade, 1927), S. tereticaudus, 3.7 g (range 2.7 to 4.7 g), and S. harrisii, 3.6 ¢ (range 3,0 to: 4.1), (Neal, 1965). Figure 1 shows growth in body weight of young Richardson ground squirrels plotted on a logarithmic scale. The instantaneous growth rate (IGR) varied from week to week, being the most rapid immedi- ately after birth and declining with age. During the first week after birth, weight increased about 11.4% per day, whereas at three weeks of age it increased 7.0% per day and at 10 weeks 2.0% per day. Neal (1965) found that the IGR of body weight in S. tereticaudus was 11.0% per day shortly after birth and dropped to 0.53% per day at 84 days of age and in §. harristt was 9.3% per day shortly after birth and dropped to 0.16% per day at 77 days of age. Figure 2 shows the rate at which adult weight and measurements were achieved in Richardson ground squirrels. ‘Twenty-five per cent of weight growth is completed by the 35th day, 50% by day 49, 75% by day 60, 90% by day 75 and 100% by the 100th day. In S. tereticaudus, 25% of weight growth is completed by 34th day, 50% by day 50, 75% by day 68 and 90% by day 79, and in S. harrisii, 25% of weight growth is completed by day 38, 50% by day 56, 75% by day 75 and 90% by day 150 (Neal, 1965). Weight and measurements taken from wild young at the time of their first emergence from their nest burrows, compared with weights and measurements of young Richardson ground squirrels raised in captivity, suggested that the wild young were about 5 to 6 weeks of age. As pointed out by Neal (1965), field weight is highly sensitive to food supply and environmental stress; growth therefore can be assumed to be somewhat more rapid in the laboratory than in the field. INCREASE IN LINEAR MEASUREMENTS Figure 3 presents the growth of the right hind foot, tail length and total length of young Spermophilus richardsoni elegans raised in cap- 281 202 Tue AMERICAN MIDLAND NATURALIST 83 (1) tivity. The hind foot growth rate is generally the most rapid, with the tail growth rate next. During the first two weeks after birth the growth rate of the right hind foot was 7.76% per day; that of the total length was 5.49% per day and of the tail 5.48% per day. Spermo- philus tereticaudus during the first two weeks of age gained 5.7% per day for tail growth, 4.9% per day for the hind foot growth and S. harrisii gained 4.9% per day for tail growth and 4.8% per day for the hind foot. The hind foot attained 25% of maximum growth at 7 days, 50% at 16 days, 75% at 26 days, 90% at 35 days and 100% at 42 days. In total length the 25% point of maximum growth was obtained in 7 days, 50% in 20 days, 75% in 37 days, 90% at 46 days and 100% at 63 days. Twenty-five per cent of maximum tail growth was reached in 10 days, 50% at 26 days, 75% at 39 days, 90% at 45 days and 100% in 56 days. In S. tereticaudus, the hind foot attained 50% of maximum growth in 22 days and 90% in 66 days, and in S. harrisii, the hind foot reached the 50% point in 23 days and the 90% in 65 days. Tail mea- surements in S. tereticaudus attain the 50% point in 27 days and 90% in 210 days, whereas S. harrisii attained the 50% in 30 days and 90% in 217 days (Neal, 1965). DiscussION Information on various aspects of growth and development of several species of Spermophilus, including S. harrisii, S. townsendi, S. richardsoni, S. columbianus, S. undulatus, S. tridecemlineatus, S. PERCENT OF ADULT SIZE AGE IN DAYS Fig. 2.—Increase in weight and measurements of young Spermophilus rich- ardsoni elegans raised in the laboratory in terms of per cent adult weight and measurements at the indicated ages. 282 1970 Crark: EARLY GROWTH OF GROUND SQUIRREL 205 spilosoma, S. beecheyi, S. tereticaudus, and S. lateralis has been given by several authors (Neal, 1965; Svihla, 1939; Denniston, 1957; Shaw, 1925; Mayer and Roche, 1954; Bridgewater, 1966; Blair, 1942; Tomich, 1962; McKeever, 1964). These data, although not complete in all cases, permit at least a gross comparison of development and growth rates of a group of species of varying habits and habitats. Juvenile ground squirrels emerge from their nest burrow with certain characteristics for survival already developed. At the time of emergence locomotor abilities, vocalizations, eye and ear opening, acquisition of teeth, ability to “bottle brush” the tail and evert the anal glands are usually accomplished. Ground squirrels that hibernate have a more rapid developmental rate during growth than non- hibernating ground squirrels of the same general size (Neal, 1965). Table 2 demonstrates this difference in growth rates and development between hibernators and nonhibernators. Acquisition of hair on head, eruption of lower and upper incisors, first trill, body fully covered = 301 zZ = 20 w Z wa 100 [+ 4 90 2 < 60 008 .003 006 .022 .O1S - s 50 ga, 039.020 020 - 5 (018 022.005.0004 .0006, of q wi Zz = a AGE IN DAYS Fig. 3.—Growth in total length (top curve), tail (middle curve), right hind foot (bottom curve) and tail (bottom curve) of young Spermophilus richardsoni elegans raised in captivity. Values above segments of curve are instantaneous growth rates. The value times 100 equals the percentage of increase per day during a particular age period. 283 83(1) THE AMERICAN MIDLAND NATURALIST 204 (F961 ‘1aAeayOW{) H aa . TE-Le cl cI aa nae 8 5101940) ° (S961 ‘Te9N) H cE 1G LG=GG 1d ° iG lL 7 Snj2ajFau snpnvIija1a} ° (2961 ‘yoruro y ) éH ¥L-09 86-FG LE-vE 0d 8C 1c €1 1494999q al TS —_ 96-06 VGEGG O§-Ge 92-06 a) ie (6F61 “T[arung) (Zr6T ‘areIg) HN 8F 86-L¢ FS . oa _ 4olvu pwosojids (9961 ‘toremosprig ) H 66 E6716 8 Gl 61-91 Laleeval v SNIDIUIWAIIPIAY (FG61 “OyIoy % Ide) H 6G aa 06 Or 8I ee on SISUaIMOLIDG SnyvjnpuN * (¢z61 ‘Meys) H O€ €¢c-61 L al 61 4q 6I-FT ft Snupiquinjor H CE-8C 9c-I¢ TGalG Co ial 90°C PI-st OT Sud a]a 1UOSPLDY IIL * ,uado sada (661 “eIytAS) H Ja}fe “OOS, , cc 6l 9T QT 8 ipuasumo} ° (S961 ‘Ie2N) HN 6F BC-1? PE-66 SGale 8C 8¢ IZ tl LISTLADY 1ISTLLDY * Bo ea se) 7 x = 55 5 ° 8 oG <& oe ag a. as eyes a: a Le oe a g 3 a 5 3 Fo 7 2 Se aie BS 3 8 g a7 Sg 28 a: BOR Se a a E ony oY) SdaYnNLVat HLMOUD ANV IVLNANdOTAAYC Yliq Vouls shep oie sIoqUINNY ‘SuDsaj]a luOspavy IIL “S) YUM sinjeIo}] 94} Ut poyodos se snprygowsadg Sunod jo sayer yIMOIS pue jusudojaaap oy} jo uostuedwon—'z alavy, HD WH HH WH WH WH 284 1970 Criark: EARLY GROWTH OF GROUND SQUIRREL 205 with short hair, eye and ear opening, and weaning appear to occur earlier in hib« srnating than in nonhibernating ground squirrels / | 9 - (able. 2): Although data exist on coe 10 of the 28 species of ozone squirrels, the foregoing comparison indicates that hi F ively more rapid rate than nonhtbernators. The relat and development of hibernating ground squirrels have mtive significance. This not oniy proban:y of time young must remain oe to the nest but also may aliow tor the eariier acquisition of the necessary motor and benaviorai agility required to survive abovezround. An ae rated ontoveny would con- ceivably be a distinct advantage to hibernating ground reis that have to grow rapidly and store an lin ited amount of time in order to survive ihe Acknowlcdoments.—1 wish to Mclaucl lin, and J. A. Swatek for Are Cis Bia, F. VW. 1942. Rate of development of young spotted ground squirrels. /. LA ¢ 23 :342-343, Baipczwsten, D. D. 1966. Laboratory breeding, carly srowth development and behavior cf Citellus tridecemlinzatus (Rodentia). Southwestern Natur., 213:3325-337 Bropy, §. 19-5. ime relations of growth of individuals and populations, p. 487-574. in 5. Brody, Bioenergetics and growth. Reinhold, New York. O23. 9: Denniston, R. H. 1957. Notes on breeding and size of young in Richardson ground squirrel. J. Mammal., 38:414-416. Hatt, E. R. anp K. Ketson. 1959. The mammals of North America. Ronald Press, New York. 1083 p. Maver, W. V. ano E. T. RocuHe. 1954. Dev elopme nt patterns in the Barrow eround squirrel, Spermophilus undulatus barrowensis. Growth, 18: 53-69. Wek 5S. 1964. The biology of the golden-mantled ground squirrel. Ecol. Monogr., 34:383-401. Neat, B. J. 1965. Growth and development of the round-tailed and Harris antelope ground squirrels. Amer. Midl. Natur., 73:479-48 SHaw, W. T. 1925. Breeding and development of the Columbian ground squirrel. J. Mammal., 6:106-113 SumRE LL, F. 1949. A life history study of the ground squirrel (Citellus spilo- soma major (Merriam)). M.S. thesis, Univ. of New Mexico, Albu- querque. Sviata, A. 1959. Breeding habits of Townsend’s ground squirrel. Murrelet, 20:6-10. Tomicu, P. Q. 1962. The annual cycle of the California ground squirrel, Citellus beecheyt. Univ. California Publ. Zool., 65:213-282. Wapbe, O. 1927. Breeding habits and early life of the thirteen-striped ground squirrel, Citellus tridecemlineatus (Mitchell). J. Mammal., 8:269-275. SUBMITTED 21 AucusT 1968 ACCEPTED 6 DECEMBER 1968 285 Article IX.—CRANIAL VARIATIONS IN NEOTOMA MICROPUS DUEL “TO GROWTH AND INDIVIDUAL DIFFERENTIATION. By ]. A. ALLEN, EAE LE In view of the stress naturally, and very properly, laid upon the importance of cranial characters in the discrimination of species in groups of closely-allied forms, it seems desirable to ascertain the character and amount of change in not only the general form of the skull but in the form of its separate bones due to growth, and also to determine the amount and kind of individual variation that may be expected to oceur in skulls unquestionably of the same species. Having of late had occasion to examine a large amount of material relating to the genus Neotoma, the subject has been forcibly brought to my attention, and some of the results of a careful examination of a large series of skulls pertaining to several species of this genus are here presented. No attempt is made to treat the subject exhaustively, only a few special points being here presented. As is well known to all experienced workers in mammaiogy, the general contour of the brain-case, the relative size and form of individual bones, notably the interparietal, and the condition of the supraorbital and other ridges for muscular attachment, alter materially after the animal reaches sexual maturity; the deposition of osseus matter, the closing of sutures, the building out of crests and rugosities continuing throughout life, so that a skull of a very old animal may differ notably from that of an indi- vidual of the same species in middle life, and this latter from one just reaching sexual maturity. ‘The Museum has at present a large series of specimens of Neotoma micropus Baird, including ages ranging from nursling young to very old adults. They are mainly from three localities in the eastern coast district of Texas, namely, Brownsville, Corpus Christi, and Rockport. In order to avoid any complications that 233 286 234 Bulletin American Museum of Natural History. [Vol. VI, might arise through geographic variation, only the specimens from Rockport and Corpus Christi—localities less than twenty-five miles apart, and similar in physical conditions—are here consid- ered. There is not the slightest reason for questioning their con- specific relationship. ‘The series selected to illustrate variations due to age are, with one exception, from Rockport ; those figured to show individual variation are all from Corpus Christi. VARIATIONS DUE TO AGE. General Contour.—The variation in the general form of the skull resulting from growth is due mainly to the lengthening of the several skull segments without a corresponding relative in- crease in the breadth of the skull. Hence in the young skull, in comparison with an adult skull of the same species, the brain- case 1s disproportionately large in comparison with the anteor- bital and basal portions of the skull. This is well shown in Plate IV, and in the subjoined table of measurements of three MEASUREMENTS AND RATIOS SHOWING CRANIAL VARIATIONS DUE TO AGE IN eotoma micropus. | No. |,...,| No. Ne | 5834, Ratio! 4480, | Ratio! ite Ratio! ¢ juv. 3d juv. volal | Occipito-nasal length <<.3<..4.40 030-4 31 {100 | 41 {100 | 53 {100 Length of nasals... 6.66 cas oe casas os 10 32.31 14.5! 85.4) 22 | 41.5 Length: of frontaiscin. Wecs ounces / 138 | 42 15 36.6] 18 | 34 Length of parietals on n median line. ...| 5 19.4] 6 14.6} 8 15 Greatest length of parietals............ | 12 39 15 36.6] 16 30.2 Leneth of interpametal. 22.5.5: 4) sc ) 4,0) 22.5) Doo) Ted) 7 13.2 eneth of brain-case...2.4.65 <2.00s4| 14 45.2) 17 | 41.5) 21 39.6 Greatest rostral breadth, .i:04. «a.a.e-, | 5.90) VT. 6.3) 1.4) 6.5) 12.8 Least interorbital breadth.. ....... re ed), 19.4] 6 14.6} 6 Pike Breadth of brain-case .. ............. 16 51.6] 19.5) 45 20 | 38 Breadth of interparietal)...< a... nsrela aa | 11 35.5) 10 24.4) 7.5) 14.2 Greatest zygomatic breadth............, 202 | 64.6) 23 56.1) 30 56.6 Depth of skull at middle of palate...... | 8 26 11 26.8 15 | 28.5 Depth of skull at front of basisphenoid.| 11 35.5) 12 | 29.3) 14 | 26.4 Length of tooth-row (crown surface)....| 8? | 25.8] 8 1950). OO), 17 Length of incisive foramina ....... <2) 6 1953) 48.5) 20.7!) 11.5) 21.47 Width of incisive foramina........... 3 9.7) 3 7.8) 8.5! 6.6 Length of ee HOOP 6 sisidn cts a, apenas 5 16.1) 7 Ly 7 | 13.2 1 Ratio to pei tere) length. ? From No. 4482, ¢ juv., in which the last molar has just come into use, 287 1894. | Allen, Cranial Variations in Neotoma micropus. 935 specimens of V. micropus from Rockport, Texas. No. 5834, Q juv., is a nursling so young that the last molar is still wholly enclosed in the jaw;' No. 4480, 4 juv., though not quite full- grown, would pass as a ‘young adult’; No. 4478, 2 ad., is a very old male, with the teeth well worn down, and the fangs visible at the alveolar border. Other specimens in the series furnish a complete series of gradations between the two extremes (Nos. 5834 and 4478). In general contour (Figs. 1-11, Pl. IV), the young skull, in comparison with adults, is much more convex in dorsal outline,” very broad posteriorly, and very narrow anteriorly. In compar- ing the relative length of the several skull segments the occipito- nasal length is taken as the basis, and the skulls will be referred to as A (=No. 5834), B (=No. 4480), and C (=No. 4478). Rostral Segiment.—In A the ratio of the rostral segment to the total length. 1s 32.3: percent.; im 4, 35.4; im C,45.5—piving a rapid /vcrease in the ratio with age. Frontal Segment.—In A the ratio of the frontal segment—v. ¢., the distance between the naso-frontal and fronto-parietal sutures —to the total length is 42. per cent.; in 4, 36.6; m C, 34—a considerable decrease in the ratio with age. Parictal Segment.—I\n A the ratio of the parietal segment— ?.e., the distance from the latero-anterior angle of the parietal bone on either side to the occipito-parietal suture—to the total length is 39 per cent.; in B, 36.6; in C, 30.2—again a rapid decrease in the ratio. Brain-casc.—The length of the brain-case in 4 Is 51.6 per cent. of the total length of the skull ; in B, 45 ; in C, 38. In each case the change in ratio is due to the disproportionate growth of the rostral portion of the skull. Thus in 4 the nasals have a length of only 10 mm.; in Z they have increased to 14.5 mm., and in C to 22 mm., while the total occipito-nasal length of 1 The length of the tooth-row given in the table is taken from an older specimen (No. 4482, 9 juv.), in which the last molar has reached the level of the others and is just beginning to show traces of wear. 2 In Figs. 10 and rt it should be noted that the greater flatness of the skull interorbitally, as compared with Fig. 6,is masked by the raised supraorbital borders in the older skulls when viewed in profile. 288 236 =Bulletin American Museum of Natural History. {Vol. VI, the skull has increased only from 31 mm. in 4 to 53 mm. in C. In other words, the nasal bones have increased in length 120 per cent., while the total length has increased only 77 per cent. Transverse Breadth.—In respect to the breadth of the skull the variations with growth are much less than in its length. Thus the greatest diameter of the rostrum varies only from 5.5 mm. in 4 to 6.5 in C—an increase of about 20 per cent. in the breadth of the rostrum, against an increase of 120 per cent. in its length. ‘The interorbital breadth remains nearly constant, being 6 mm. in all three of the skulls here compared. The width of the brain-case shows an increase of 25 per cent. against an increase in the total length of the skull of 77 per cent. The zygomatic breadth shows an increase of about 50 per cent., due almost wholly to the thickening and increased convexity of the zygomatic arches. Vertical Depth.—In respect to the depth of the skull, the vari- ations with age prove especially interesting, although only such as would be expected from the facts already given. For present purposes the depth of the skull is taken at two points, namely, (a) at the middle of the palatal region, and (4) at the posterior border of the basisphenoid (basisphenoid-basioccipital suture). The palatal depth increases markedly with age, correlatively with the growth of the rostrum ; the basisphenoidal depth changes but slightly after the molars have attained to functional development. ‘Thus in 4 the basisphenoidal depth is r1 mm.; in #, 12 mm. ; in C, 14 mm.-—an increase of about 28 per cent. ‘The palatal depth in 4 is 8 mm.; in &, 11 mm.; in C, 15 mm.—an increase of nearly 88 per cent. Tooth-row.—Vhe length of the upper tooth-row varies about 12 per cent., due almost wholly to the wearing down of the teeth, the length of the crown surface being much less, in slightly worn teeth, than the length taken at the alveolar border. Luterparretal—Vhe interparietal shows surprising modification with age, both as to size and form, but especially in respect to the latter. At early stages, as in 4, this bone is more or less crescentic in shape, with the transverse diameter more than twice 289 1894.]| Allen, Cranial Variations in Neotoma micropus. 231 the antero-posterior diameter. ‘Thus in 4 the two diameters are respectively 11 and 4.5 mm.; in 4, ro and 5.5 mm.; in C, 7.5 and 7 mm. In other words, the short, broad, convex sub-cres- centic interparietal in A becomes transformed in C into a squarish, flat bone in which the two diameters are nearly equal, instead of the transverse being twice as great as the antero- posterior, as in A. ‘This would be almost incredible were not the proof so abundantly furnished by the material in hand, where every stage of transition is shown. (Figs. 1-8, Pl. IV.) This change is coincident with the development of the raised supra- orbital borders and their prolongation backward as ridges to the parieto-occipital suture, and the flattening of the whole dorsal aspect of the post-rostral portion of the skull. In old age these ridges become confluent with the lateral edges of the interparietal which has now lost its postero-lateral moieties, partly apparently by absorption and partly by their being overgrown by the mediad posterior angle of the parietals. A sharp thin ridge for muscular attachment also extends back from the posterior base of the zygomatic arch. ‘he interparietal at the same time develops a more or less prominent median angular projection at its posterior border, confluent with the median ridge of the supraoccipital. The contrast between these conditions, obtaining only in very old skulls, and their almost entire absence in skulls which have just reached sexual maturity, is strikingly great. Supraoccipital —The supraoccipital changes from a posteriorly convex, thin lamina of bone, in early life, to a thick, nearly ver- tical plate, with a strongly-developed median ridge produced into an angular spine at its superior border, and with a lateral ridge on either side about midway between the median line and its lateral borders ; these lateral ridges also each develop an angular rugosity or process about midway their length. The superior border is also produced into an incipient occipital crest. Bastoccipital.-—The basioccipital becomes greatly altered by growth, as in fact is the case with the whole postpalatal region. In comparing stages 4 and C it is found that the distance across the occipital condyles increases only about 15 per cent., while the breadth of the anterior border increases roo per cent., and the length about 50 per cent. (Figs. 12-14, PJ. IV.) 290 238 Bulletin American Museum of Natural History. {Vol. VI, Basisphenoid.—The basisphenoid doubles in length, and its anterior third becomes differentiated into a narrow projecting neck. ‘The presphenoid at stage A is nearly hidden by the palatal floor. (Figs. 12-14, Pl. IV.) Postpalatal Region as a whole.—This doubles its length with an increase in breadth of only about 50 percent. At stage A the postpalatal border terminates slightly behind the posterior edge of M.2; in stage 3 it holds very nearly the same position. The distance between the postpalatal border and the front border of the auditory bullz, compared with the total length of the skull, isas1togin A,andasito5inC. In J the pterygoid hamuli reach the second fourth of the bulle; in C they terminate slightly in advance of the bulla. The bulle themselves in 4 are more obliquely placed than in C, in relation to the axis of the skull, and are quite differently shaped. Also the form of the foramen magnum has undergone much change. These points are all well shown in Figs. 12-14 of the accompanying plate. Lnetsive Foramina.—Consequent upon the growth of the rostral portion of the skull, the incisive foramina undergo marked change in form, and somewhat in position, as regards both their anterior and posterior borders. In the stage designated as 4 they are short and broad, and extend relatively further both anteriorly and posteriorly than in stage @ or C, their anterior border being nearer the base of the incisors, and their posterior border being carried back to or slightly behind the front border of the first molar. Thus in 4 the length of the incisive foramina is 6 mm., with a maximum breadth of 3 mm., while in C the dimensions are respectively 11.5 and 3.5 mm.—a great increase in length with only slight increase in breadth. At the same time the anterior border is considerably further from the base of the incisors, and the posterior border is slightly in advance, instead of slightly behind, the front border of the molars. Spheno-palatine Vacutties.—In adults of Veotoma micropus, as in other species of the ‘ round-tailed’ section of the genus, there is a long, broad vacuity on each side of the presphenoid and ante- rior third of the basisphenoid, which Dr. Merriam has recently 291 1894.]| Allen, Cranial Variations in Neotoma micropus. 239 named’ the ‘ spheno-palatine vacuities,’ and he has also called atten- tion to the fact that they are not present in some forms of the ‘bushy-tailed’ section of the genus. It is therefore of interest in the present connection to note that these vacuities are absent at stage 4, and are only partially developed at later stages (Figs. 12-14, Pl. lV). My attention was called to the matter by finding several nearly fully-grown skulls from Texas and northeastern Mexico with these vacuities either quite absent or represented by an exceedingly narrow slit, while I could find no differences in the skins or in other cranial characters that gave the slightest hint that the animals were not referable to V. mzcropus. Further examination of young skulls of undoubted VV. mzcropus from Rockport and Corpus Christi, Texas, showed that the closed condition was in this species a feature of juvenility. It is thus of interest to find that a feature which proves to be merely a char- acter of immaturity (and quite inconstant as well) in JV. mzcropus is a permanent condition in JV. cinerea occidentalis.” In the development of these vacuities it appears that as the presphenoid increases in length it becomes reduced in width ; at the same time, as the skuil broadens, the edges of the ascend- ing wings of the palatine bones become slightly incised. There is, however, much individual variation in this respect, as will be shown later. Molars.—When the molars first cut the gum they have nearly the entire crown-surface capped with enamel. Very soon, even before the tooth has attained its full height, the enamel begins to disappear from the centers of the enamel loops, the capping re- maining longer over the narrower loops than over the broader ones; it quickly disappears from all as soon as the crown-surface becomes subject to wear. In stage 4,1in which only M.1 and M.2 have appeared, and are less than one-third grown, the enamel walls of the loops nearly meet over the dentinal areas— quite meeting over the narrower portions, especially in the case of the middle transverse loop of each tooth. Some time before the age represented by #@ is reached, the crown-surface is worn to an 1 Proc. Biol. Soc. Wash., VIII, p. 112, July, 1893. 2 Unfortunately the outline figures here given (Figs. 12-15, Pl. 1V,) fail to show clearly the points at issue. 292 240 Bulletin American Museum of Natural Hrstory. {Vol. VI, even plane; the tooth has reached its normal length, but the fluting of the sides still extends to the alveolar border. As attrition goes on, with the advance of the animal in age, the crown-surface wears down, and the neck of the tooth appears above the alveolar border, till, especially in the upper molars, the fluted terminal and the smooth basal portions are of nearly equal extent; but in old age (as in C’) the smooth basal portion is the longer and the division of the root into fangs is clearly shown. With this wearing down the tooth increases somewhat in both width and length, but the pattern of the enamel folds undergoes but shght change until nearly the whole crown is worn away, except that the angles become gradually more rounded. Résumé.— As already stated the change with age in the general form of the skull is due to the relatively disproportionate increase in length of the pre- over the post-orbital region, and the same disproportionate increase of the basal region as compared with the frontoparietal elements. In the first case the rostrum be- comes relatively greatly produced ; in the second the basiocci- pital and adjoining parts become so greatly enlarged as to change the entire aspect of the basal region of the skull. Thus the occipital condyles, which in A terminate slightly in advance of the most convex portion of the supraoccipital, and are crowded up very close to the bulla, form in C the most posterior part of the skull, with a considerable interval between them and the billess Chiesa —e4, Ply s) INDIVIDUAL VARIATION. In comparing a large series of skulls of the same species it quickly becomes apparent that no element of even the adult skull is constant, either as to form or relative size. There is also much variation in the size of skulls of the same sex and approxi- mately the same age. Variation in Sise—Thus in Meotoma micropus, from the same locality, there are dwarfs and giants. While the females average smaller than the males, size is by no means a safe criterion of sex. Thus two old females, not appreciably different in age, from Corpus Christi, Texas, vary as follows: No. 2948, total 293 1894.| Allen, Cranial Variations in Neotoma micropus. 9Al length 51 mm., zygomatic breadth 26 mm.; the corresponding dimensions in No. 2955 are 45 mm. and 24 mm. These are merely the extremes of a series of six specimens; with a much larger series doubtless the difference would be considerably increased. A series of six old males, from the same locality and indistinguishable as to age, vary as follows: No. 2952, total length 50.5 mm., zygomatic breadth 27 mm. ; the corresponding dimensions in No. 2956 are 45 mm. and 25 mm. Nasals and ascending branches of the Premaxille.—Ordinarily in JV. micropus the nasals terminate in a gradually narrowed evenly rounded point, a httle less than 2 mm. in front of the posterior termination of the ascending branches of the premaxille. The distance between the points of termination of the nasals and premaxillz, however, frequently varies between 1.5 and 2.5 mm.; more rarely from 1 to 3 mm. These extremes each occur in the ratio of about 1o percent. of the whole, while probably 60 per cent. would not vary much from the normal average of about 2mm. (See Figs. 1-8 and 16, 17, Pl. IV.) The nasals, as already said, usually terminate in an evenly rounded point, but in several of the 50 skulls of WV. micropus before me their posterior border forms a double point, each nasal terminating in a distinctly rounded point; in one or two the posterior border is squarely truncate; in others it is irregularly uneven. The ascending branches of the premaxille usually terminate in an obtusely V-shaped point, with a uniformly even outline, their breadth, however, being subject to variation; in some specimens they terminate in a brush of irregular spicule. (Figs. 1-8 and 16, 17, Pl. IV.) Frontals.—TYhe posterior border of the frontals is subject to great irregularity, varying from a nearly transverse line (rounded slightly at the outer corners) to a gentle, rather even convexity, and thence to an acute angle, involving the whole posterior border. It is difficult to decide what outline is the most frequent, though the tendency seems to be greatest toward a well-pro- nounced rather even convexity. Figures 1-8 and 18, 19, Plate V, well show the variation in the position and direction of the fronto-parietal suture. | September, 1S94. | 294 242 Bulletin American Museum of Natural History. |Vol. V1, Parietals.—The anterior outline of the parietals of course con- forms to the posterior outline of the frontals, and must be equally variable. It hence follows that their length on the median line is also variable. Their posterior border is also subject to much variation in consequence of the great diversity in the form of the interparietal. Interparietal——In middle-aged specimens the interparietal tends strongly to a quadrate form, varying from quadrate to diamond shape, through a more or less marked median angular extension of both its anterior and posterior borders, and occasionally of its lateral borders as well. Often it forms a quadrate figure, in which each of its four sides is slightly convex ; again the corners are so much rounded, and the lateral breadth so much in excess of the antero-posterior, as to give a lozenge-shaped figure. In other cases it is distinctly shield-shaped ; in others it is hexagonal. In size the variation is fully 50 per cent. of what may be regarded as the average dimensions. These remarks have strict reference to fully adult specimens, and as nearly as can be judged these variations are not at all due to differences of age, which, as already shown, has so great an influence upon the size and form of this exceedingly variable element of the skull." (Figs. 20-23, Pl. IV. Compare also the interparietal, as shown in Figs. 1-8.) Ventral aspect—The ventral aspect of the skull presents numerous points of variability, only a few of which will be here mentioned. The palate varies more or less in breadth, and especially in the development of the anterior palatal spine, which is sometimes slight, and sometimes so strongly produced anteri- orly as to touch the vomer. The postpalatal border may be evenly concave, or present a slight median process. The pre- sphenoid is very variable in size, being often an exceedingly slender rod of bone, and at other times very stout, the variation in thickness being nearly or quite 100 per cent. The anterior third of the basisphenoid shares in the same variability. As the 1 As regards variation with age in the form of the interparietal, Neotoma micropus is only an example of what doubtless prevails throughout the genus, and even in many other genera as well. Yet in adult animals the form of this bone seems, as a rule, to be sufficiently constant to be of more or less taxonomic value. Thus in the \. c7xerea group it may be said to be nor- mally quadrate ; in the V./usczpes group it is quite constantly ehicic chaped In NV. floridana, however, and in the WV. szexicuma group, it seems to be nearly or quite as variable as in V. micropus, both as to size and shape. 295 1894. | Allen, Cranial Variations in Neotoma micropus. 243 ascending borders of the palatals are also variable in respect to the extent of their development, it follows that there is, even among adults, a wide range of variation in the size of the spheno- palatine vacuities. Teeth.—Aside from differences due to age and attrition, the teeth vary in size to a considerable extent among individuals strictly comparable as to sex and age, some having a much heavier dental armature than others. But more particularly note- worthy in this connection is the variation in the color of the teeth, which seems strongly a matter of individuality. Although Dr. Merriam has recently placed JV. micropus in his “‘ Meotoma leucodon group,’ which has, among other alleged characters, “color of teeth white or nearly white,” the teeth in V. mcropus average blacker than in any other species of the genus known to me. Were this all it might be considered that WV. micropus was erroneously referred to the ‘Zeucodon group’; but unfortunately the range of individual variation in the color of the teeth in the large series at hand covers also the whole range of variation for the genus. Thus in some instances the molar teeth are intensely black from base to crown, while the crown-surface itself is strongly blackish, even the enamel loops, as well as the enclosed dentine being tinged with blackish ; in other cases the teeth are merely slightly tinged with brownish near the base and at the bottom of the sulci. These extremes are connected by a series of very gradual intergradations. In other words, among hun- dreds of skulls of Veotoma, those with the blackest teeth occur in WV. micropus, as well as those in which the teeth are practically white. In the suckling young the teeth are pure white; before M.3 has come to wear, M.1 and M.2 have become more or less blackened ; in young adults, and in middle aged specimens, the teeth are often intensely black; in old specimens, with the teeth much worn, the teeth average lighter than in the younger indi- viduals. There is, however, a wide range of variation in the color of the teeth in specimens of corresponding age, whether old or young. The black coloring consists to a large extent of a 1 Proc. Biol. Soc. Wash., IX, p. 118, July 2, 1804. 296 244 = =Bulletin American Museum of Natural History. (Vol. VI, superficial incrustation which tends to scale off in flakes in the prepared skull, and its absence apparently may be due sometimes to removal in the process of cleaning the skull for the cabinet. In other words, the blackness is to some extent an accidental or pathological condition, due probably more or less to the particu- lar character of the food or to the health of the animal. GENERAL REMARKS. The bearing of what has been stated above respecting varia- tions in the form of the skull and of its principal elements due to age is of course obvious, the inference being that in animals which have reached sexual maturity variations due wholly to growth, in passing through adolescence to senility, may readily be mistaken, when working with very small series or with single specimens, for differences of subspecific or even specific import- ance. Not only do the individual bones vary in their outlines and proportions and in relative size, but the skull varies as a whole in its relative dimensions, including depth as well as length and breadth. ‘There is beside this a wide range of purely indi- vidual variation, affecting every character that can be used ina diagnostic sense. Thus in a series of fifty skulls of Meotoma micropus it would be easy to select extremes, of even individual variation, that depart so widely from the average, in one or more characters, as to deceive even an expert, on considering these alone, into the belief that they must represent very distinct species ; yet in the present instance the proof that such is not the case is overwhelming. In JW. micropus the coloration is re- markably constant, for a member of this genus, at all seasons and ages, so that the case is less complicated than it would be in many other species of the group, where the color of the pelage varies radically with season and age. Personal criticism is not the purpose of the present paper, and it was not my intention at the outset to refer specifically to the work of any of my confréres. Since its preparation was begun, however, its razson @’étre has perhaps been emphasized by the pub- lication of two brochures of ‘ preliminary descriptions’ of species and subspecies of the genus MWeofoma, numbering altogether ro species and 8 subspecies, which added to the 22 species and sub- 297 1894. | Allen, Crantal Variations tn Neotoma micropus. 245 species previously standing practically unchallenged, makes, at the present writing, a total of 4o forms of the genus /Veotoma. Of these no less than 26 have been described within the last nine months.’ Without the material before me used by the original describers of these forms it would be presumptive to give an opinion respecting the merits of many of them. While the greater part may have some real basis, it is evident that others are almost unquestionably synonyms of previously-described forms, judging by ‘topotypes’ in this Museum, the brief diagnoses accompanying the names affording in these cases no characters that are in the least degree distinctive. The genus /Veotoma was chosen for treatment in this connec- tion in preference to some other almost solely by chance, as the facts of variation above presented are not at all exceptional. In fact the common muskrat (fiber zibethicus) would have shown a still more striking case of variability, as would also various species of many other genera. Yet describers of new species are con- stantly laying stress upon cranial differences that have not neces- sarily the slightest specific or even subspecific importance ; and, so far as can be judged from their descriptions, they are entirely unconscious that such can be the case. On the other hand, it 1s equally certain that such alleged characters may have the value assigned them; since it is now a well known fact that the extremes of purely individual variation in any character, external or internal, may exceed in amount the average differences that serve to satisfactorily distinguish not only well-marked subspecies, but even forms that are unques- tionably specifically distinct. Hence it must often happen that the determination of the status of a species or subspecies origin- ally described from one or two specimens, in groups especially susceptible to variation, must depend upon the subsequent exam- ination of a large amount of material bearing upon this and its closely-related forms. 1 For a list of the species and subspecies of Meofoma described prior to July 6, 1894, see Abstr. Proc. Linn. Soc. New York, No. 6, pp. 34, 35, July, 1894. 298 246 Bulletin American Museum of Natural History. |Vol. V1.) EXPLANATION OF PLATE IV. Figures all Natural size. Neotoma micropus Saird. Showing cranial variations due to age and individualism. (Unless otherwise stated, the specimens are from Rockport, Texas. ) Figs. 1-8. Dorsal aspect of skull, showing gradual change in form with age, and especially in the form and relative size of the interparietal. Fig. 1, No. 5834, @ juv. (suckling). Fig. 2, No. 2975, @ juv. (nearly sexually adult), Corpus Christi, Texas. Fig. 3, No. 5841, @ ad. Fig. 4, No. 4480, ¢ ad. Fig. 5, No. 2958, 6 ad,, Corpus Christi. Fig. 6, No. 4479, 6 ad. Fig. 7, No. 4477, @ ad. Fig. 8, No. 4478, 6 ad. Figs. g-11. Skull in profile, to show change of form with growth. Fig. 9, No. 5834, ¢@ juv. (nursling). Fig. 10, No. 4480, 4 ad. (rather young). Fig. 11, No. 4478, 4 ad. (very old). Figs. 12-15. Ventral aspect, showing variations in postpalatal region due toage. Fig. 12, No. 5834, @ juv. (nursling). Fig. 13, No. 5841, ? ad. (young adult). Fig. 14, No. 2958, Corpus Christi, ¢ ad. (very old). Fig. 15, No. 1456, Meotoma cinerea occidentalis, 6ad., Ducks, B. C. (for comparison with NV. micropus). Figs. 16, 17. To show extremes of individual variation in relative posterior extension of nasals and ascending branches of premaxillz. Locality, Corpus Christi, Texas. Fig. 16, No. 2958, 4 ad. Fig. 17, No. 2948, & ad. Figs. 18, 19. To show extremes of individual variation in posterior border of frontals. Locality, Corpus Christi, Texas. Fig. 18, No. 2949, 4 ad. Fig. Ig, No. 2951, 6 ad. Figs. 20-23. To show individual variation in the size and form of the inter- parietal. Specimens all from Corpus Christi, Texas. Fig. 20, No. 2949, ¢ ad. Fig. 21, No. 2948, @ ad. Fig. 22, No. 2952, 4 ad. Fig. 23, No. 2945, ¢ ad. Nore.—If the Brownsville, Texas, series of specimens had also been included, the range of individual variation would have been considerably increased. 299 300 MATURATIONAL AND SEASONAL MOLTS IN THE GOLDEN MOUSE, OCHROTOMYS NUTTALLI DonaLp W. LINZEY AND AticiA V. LINZEY ABsTRACT.—The adult pelage of the golden mouse (Ochrotomys nuttalli) is attained by a single maturational molt. Data on the post-juvenile molt were obtained from 96 young golden mice. This molt began on the ventral surface and spread dorsally, meeting in the dorsal midline. It then proceeded anteriorly and posteriorly. The average age at which male golden mice began molting was 36 days, whereas that of females was 38 days. The average duration of molt for the sexes was 29 days and 25 days, respectively. Golden mice undergo two seasonal molts—spring and fall. Data were obtained from 36 mice. The winter pelage was generally much darker than the summer pelage. Both spring and fall molts were more irregular than the post-juvenile molt, and the spring molt tended to be more irregular than the fall molt. Young golden mice born after 1 October and 8 April appeared to combine the post-juvenile and seasonal molt. Hair replace- ment was more irregular than during the normal post-juvenile molt. During the course of a study on the ecology and life history of the golden mouse, Ochrotomys nuttalli nuttalli, in the Great Smoky Mountains National Park (Linzey, 1966), considerable data were obtained on pelage changes. The limited data presented by Layne (1960) have been the only published information concerning molt in this species. MATURATIONAL MOLT The adult pelage of the golden mouse is attained after a single matura- tional molt. Data on the post-juvenile molt were obtained from 96 young golden mice. Eighty-four of these mice were raised in captivity. Data from the remaining 12 individuals were obtained from field observations. The molt from the golden-brown juvenile pelage to the golden-orange adult pelage, although varying in details, followed a definite pattern (Fig. 1). The first indication of the beginning of the dorsal molt was the appearance of new golden fur along the line separating the golden-brown dorsal fur from the white fur of the ventral surface. The replacement of the juvenile pelage progressed dorsally on both sides and met on the dorsal midline forming a continuous band of new fur. The molt then proceeded anteriorly between the ears and onto the head, while posteriorly, it joined the molt proceeding dorsally near the thighs. By this time, new fur had appeared on the sides of the face and just anterior to the ears. The molt along the sides of the body had nearly been completed by this time. The last two areas in which the fur was replaced were the top of the head and the base of the tail. In some individuals, the new fur first appeared just in back of the front leg. It pro- ceeded both posteriorly and dorsally and formed a band of new fur just behind the ears. The molt proceeding posteriorly then covered the remainder of the body. This pattern of molt generally agrees with that described for Peromyscus 236 301 May 1967 LINZEY AND LINZEY—MOLT OF GOLDEN MOUSE 21, vy Fic. 1.—Sequence of post-juvenile molt on the dorsum in Ochrotomys nuttalli. Shaded portions represent areas of active hair replacement. Stippled areas represent adult pelage. 302 938 JOURNAL OF MAMMALOGY Vol. 48, No: 2 TasLE 1.—Duration of post-juvenile molt and average age at beginning and ending of molt in 34 captive golden mice (Range of values in parentheses). Males (15) Females (19) Duration 29 days (1445) 25 days (12-49) Beginning 36 days (33-42) 38 days (31-47) Ending 64 days (51-87) 63 days (51-84) truei (Hoffmeister, 1944), Peromyscus gossypinus (Pournelle, 1952) and Peromyscus boylei (Brown, 1963). It differs from that reported for Pero- myscus leucopus noveboracensis (Gottschang, 1956). Data on the beginning, ending, and duration of the post-juvenile molt on the dorsum in male and female golden mice are compared in Table 1. The average duration of molt for males was slightly longer than for females. The shortest time recorded was between 12 and 14 days, whereas the maximum time required was about 49 days. Approximately 3.5 weeks are required for most Peromyscus leucopus noveboracensis to attain their full adult coat according to Gottschang (1956). He recorded a minimum duration of 12 days for captive individuals and 10 days for one wild mouse to undergo the com- plete molt; the maximum number of days required was about 36. In the field, animals undergoing various stages of maturational molt were recorded in June (1), July (1), August (2), and December (8). These mice were between 150 mm and 164 mm in total length (mean, 156 mm). In the captive population, male golden mice began molting when their total length was 149 mm, whereas females averaged 146 mm. At the completion of molt, their measurements averaged 163 mm and 160 mm, respectively. From these data, it appears that both wild and captive individuals molted at approxi- mately the same body size, although it is not known whether they were the same age. The youngest individuals in captivity to begin molting during the current study were 31 days of age. Layne (1960) recorded one young Ochrotomys molting at 31 days of age with the molt apparently being complete 10 days later. Molting was in progress in one four week old mouse, while in another of the same age, it had not yet begun (Layne, 1960). Collins (1918) reported that the transition from juvenile to post-juvenile pelage in Peromyscus usually began at 6 weeks and was completed about 8 weeks later. The earliest age at which Peromyscus leucopus noveboracensis began molting was 38 days (Gottschang, 1956). These were all males. The youngest female to begin molting was 40 days of age. Ninety-five per cent of his mice of both sexes started the pelage change between the ages of 40 and 50 days. Young Pero- myscus gossypinus began molting when they were between 34 and 40 days of age (Pournelle, 1952). Gottschang (1956) found that, in general, mice of the same sex in a single litter started molting simultaneously. However, in every case where a dif- ference did occur, he found that the males started to molt first. In the current 303 May 1967 LINZEY AND LINZEY—MOLT OF GOLDEN MOUSE 239 study, the males in 13 out of 21 litters containing mice of both sexes began molting before the females, whereas the females began molting first in three litters. The initiation of molt was simultaneous in the remaining five litters. The progression of the ventral molt was studied in seven individuals (four males, three females). The white belly fur was dyed purple by the stain Nyanzol A (20 g per liter of water-hydrogen peroxide mixture in ratio of two to one) and replacement by new hairs was followed. The ventral molt began approximately 2-4 days before the dorsal molt. Hair replacement occurred first in the center of the belly and continued laterally, and then dorsally into the golden fur. Simultaneously, new hair appeared over the entire chest and abdomen. The last areas to acquire new pelage were the throat and the ventral bases of the hind limbs. The ventral molt was complete at about the time that the dorsal molt covered the entire back (Fig. 1). SEASONAL MOLT Mice of the genus Peromyscus are generally considered to undergo one annul adult molt in autumn (Collins, 1923). However, Osgood (1909) and Brown (1963) recorded two annual molts in Peromyscus melanotis and Pero- myscus boylei, respectively. Golden mice in the Great Smoky Mountains National Park apparently un- dergo two annual molts. These take place during the spring (April-June) and fall (October-December ). The difference between summer and winter pelage was clearly distinguishable with the unaided eye. The winter pelage was much darker than the usual summer pelage, especially on the mid-dorsum. Osgood (1909) noted that winter specimens of Peromyscus melanotis pos- sessed a paler colored pelage, whereas summer specimens were in a dark pelage. The fall molt of P. boylei was characterized by the replacement of a bright cinnamon-brown pelage by a more drab, brown winter pelage (Brown, 1963 ). Nineteen of 21 adult golden mice in captivity underwent a fall molt between October 20 and December 24. A total of 10 adult golden mice were observed in the wild between December 12-17. Six of these were molting; four already had the winter pelage. The fall molt appeared to be more irregular than the post-juvenile molt. In several animals, it began near the hind leg, covered the rump and then progressed anteriorly to the head. Replacement of the hair was completed first over the posterior half of the body. This separated the two remaining areas of molt—the base of the tail and the head. The replacement of fur at the base of the tail was completed shortly thereafter. The final area of molt was on the head between the ears, and this sometimes required several weeks for completion. This is in contrast to the post-juvenile molt, where the last area of molt in all of the animals was at the base of the tail. The spring molt must have occurred between 1 April and 15 June. All wild individuals observed between 26 March and 1 April 1964 still retained their 304 240 JOURNAL OF MAMMALOGY Vol. 48, No. 2 winter pelage. By 15 June, all adult golden mice had either already com- pleted their spring molt or were very near completion. Seventy-four per cent (23) of the adult individuals in the captive population molted during the spring. Of those molting, 83% (19) did so between 15 May and 30 June. As in the fall molt, the pattern was irregular. Hair replacement occurred in patches along the sides and across the shoulders, and a simultaneous molt of the entire dorsum took place in only five of 31 individuals (16%). In the cases where this molt was complete, it followed a more regular pattern, with hair replacement occurring last on the nape of the neck. Gottschang (1956) noted no difference in the onset, progress or length of time required for the pelage change between spring-, summer-, or fall-born litters of Peromyscus leucopus. During the current study, however, golden mice born after 1 October and 8 April appeared to combine the post-juvenile molt and seasonal molt. The process of hair replacement was more irregular than during the normal post-juvenile molt. The molt began at a point just behind the front legs, as in the regular post-juvenile molt. It then proceeded dorsally and posteriorly at approximately equal rates. During the combined fall molt (post-juvenile plus fall molt), the replacement of hair at the base of the tail was completed prior to the completion of molt on the head in all cases. In this respect, this combined molt was more similar to the regular seasonal molt than to the regular post-juvenile molt. Upon completion of this molt, the mice had acquired the typical dark winter pelage. However, during the combined spring molt (post-juvenile plus spring molt), hair replacement was completed last at either the tail or head regions. On the average, those animals born after 1 October began molt at a later age than did those animals born earlier in the breeding season. Males in this group began molting at an average age of 37 days, whereas spring and summer-born males began at 35 days of age. Females born after 1 October began molting at an average age of 43 days, while females born earlier in the season began molting at an average age of 37 days. ACKNOWLEDGMENTS We thank Dr. W. Robert Eadie of Cornell University for his advice and criticism of the manuscript. We gratefully acknowledge the financial assistance provided by The Society of the Sigma Xi and the cooperation of the National Park Service. LITERATURE CITED Brown, L. N. 1963. Maturational and seasonal molts in Peromyscus boylei. Amer. Midland Nat., 70: 466-469. Couuins, H. H. 1918. Studies of normal molt and of artificially induced regeneration of pelage in Peromyscus. J. Exp. Zool., 27: 73-99. 1923. Studies of the pelage phases and nature of color variations in mice of the genus Peromyscus. J. Exp. Zool., 38: 45-107. GottscHanc, J. L. 1956. Juvenile molt in Peromyscus leucopus noveboracensis. J. Mamm., 37: 516-520. HorFMEIsTeR, D. F. 1944. Phylogeny of the Nearctic cricetine rodents, with especial 305 May 1967 LINZEY AND LINZEY—MOLT OF GOLDEN MOUSE DAT attention to variation in Peromyscus truei. Ph.D. thesis, Univ. California, 406 pp. Layne, J. N. 1960. The growth and development of young golden mice, Ochrotomys nuttalli. Quart. J. Fla. Acad. Sci., 23: 36-58. Linzey, D. W. 1966. The life history, ecology and behavior of the golden mouse, Ochrotomys n. nuttalli, in the Great Smoky Mountains National Park. Ph.D. thesis, Cornell Univ., 170 pp. Oscoop, W. H. 1909. Revision of the mice of the American genus Peromyscus. N. Amer. Fauna, 28: 1-285. PourRNELLE, G. H. 1952. Reproduction and early post-natal development of the cotton mouse, Peromyscus gossypinus gossypinus. J. Mamm., 33: 1-20. Division of Biological Sciences, Cornell University, Ithaca, New York. Accepted 16 January 1967. 306 SECTION 4—ECOLOGY AND BEHAVIOR Animal behavior, or ethology, and ecology are varied and expanding fields of biology. The older term “natural history” is a concept that embraces both, and earlier “naturalists” were the pioneers of these fields. Ecology is of special importance to man owing to his increasing awareness of, and concern for, his own environment and such problems as the need to regulate human popula- tions, to reduce pollution of air and water, and to conserve endangered species. The papers selected here can suggest to the reader some basic ecological prin- ciples that apply to man himself, as well as to other mammals. Our selections illustrate concepts such as territoriality and home range (applied to mammals in the classic paper by Burt), studies that provide sound theory and quantita- tive results based on large sample sizes (Caughley), and the application of experimental procedures (as in the manipulation of rats in city blocks reported by Davis and Christian or the tests run by McCarley in compartmented cages). The application of newer techniques such as Pearson's traffic counter for mouse runways, radio-tracking techniques used by Rongstad and Tester, and other types of modern technology, including radar (Williams et al.), and even earth-orbiting satellites (Craighead et al., 1971, not included), all have con- tributed to advances in ecology and ethology. However the study by Estes and Goddard of the African wild dog will serve to remind the reader that careful observational methods such as were used so effectively by earlier field natur- alists certainly have not been supplanted, but only expanded and _ supple- mented. A host of topics other than those we were able to include in our selection come to mind when the ecological literature is contemplated—topics such as food habits as learned from stomach contents or droppings, or the extensive literature on small mammal populations (grid live-trapping, employed by Congdon, is one of the most commonly used methods). Long-term cycles in populations and daily cycles in activity have had their share of attention also, as indicated in the papers by Tast and Kalela, and by Grodzinski. Ecological problems may be approached at different levels of inclusiveness. The relationships of all species of plants and animals in an entire community may be studied; such a broad approach to entire ecosystems merges imper- ceptibly with problems concerning factors that limit distributions, hence to ranges of species and to faunal and zoogeographic problems (see Section 6). At a less inclusive level, the ecological relationships of a single species or population may be studied. These approaches are called autecology, or popu- lation ecology, as opposed to community or synecological studies. If we restrict ourselves further to the environmental relationships of individual animals, we find our studies, again by gradual stages, merge with those that are primarily physiological (see Section 2). Physiological techniques also enter directly into the study of ecosystems when energy flow is considered, as often is the case in recent studies (see, for example, Grodzinski et al., 1970). Just as ecological principles may be applied to the mammal, man, so may many cthological concepts, and part of the current interest in mammalian be- havior (Ewer, 1968) stems from this possibility. For example, our selections concerning paternal (Barlow) and maternal (Rongstad and Tester) behavior 307 (see also Rheingold, 1963) have obvious parallels in human society, and in- terpretations of observations are often controversial, as Barlow’s reply attests. Other aspects of behavior illustrated by our selections include predation or foraging (Suthers, Estes and Goddard); orientation (Suthers, Layne), social dominance (Roberts and Wolfe), and reproductive behavior (Samaras). The last-mentioned paper is of particular interest in that the observations reported raise the issue of “altruistic” or “reciprocal” behavior, concepts of great current interest (see Wilson, 1975). Ecotocy and EcotocicaL Monocrapus, published by the Ecological So- ciety of America, and the JourNAL or ANrMAL Ecotocy, by the British Eco- logical Society, are among the most important journals containing articles on mammalian ecology. Comparable journals in the field of ethology are ANIMAL Benaviour, ANIMAL BeHaviour Monocrapus, BEHAvIouR (including Supple- ments), and Zerrscurirr FUR TierpsycHoLocie. In recent years a number of new ecological journals have been established, such as Orkos and Oxcoxocr, in which papers on mammals occasionally appear. Ecological and ethological texts have also burgeoned in recent years. Those we judge to be of particular interest to mammalogists include Animal Behavior: An Evolutionary Approach (Alcock, 1975), Ecology: An Evolu- tionary Approach (Emlen, 1973), Animal Behavior (Hinde, 1970), Mechan- isms of Animal Behaviour (Marler and Hamilton, 1966), Ecology, by Krebs (1972), and Robert Ricklefs’ Ecology (1973). Many other new books in these fields, as well as older classics, will reward the student, but they are far too numerous to mention. 308 MORTALITY PATTERNS, IN MAMMALS GRAEME CAUGHLEY Forest Research Institute, New Zealand Forest Service, Rotorua, and Zoology Department, Canterbury University, New Zealand (Accepted for publication December 8, 1965) Abstract. Methods of obtaining life table data are outlined and the assumptions implicit in such treatment are defined. Most treatments assume a stationary age distribution, but published methods of testing the stationary nature of a single distribution are invalid. Samples from natural populations tend to be biased in the young age classes and therefore, because it is least affected by bias, the mortality rate curve (q,) is the most efficient life table series for comparing the pattern of mortality with age in different populations. A life table and fecundity table are presented for females of the ungulate Hemiutragus jemlahicus, based on a population sample that was first tested for bias. They give estimates of mean generation length as 5.4 yr, annual mortality rate as 0.25, and mean life expectancy at birth as 3.5 yr. The life table for Hemitragus is compared with those of Ovis aries, O. dalli, man, Rattus norvegicus, Microtus agrestis, and M. orcadensis to show that despite taxonomic and ecological differences the life tables have common characteristics. This suggests the hypotheses that most mammalian species have life tables of a common form, and that the pattern of age- specific mortality within species assumes an approximately constant form irrespective of the proximate causes of mortality. INTRODUCTION Most studies in population ecology include an attempt to determine mortality rates, and in many cases rates are given for each age class. This is no accident. Age-specific mortality rates are usually necessary for calculating reproductive values for each age class, the ages most susceptible to natural selection, the population’s rate of in- crease, mean life expectancy at birth, mean gen- eration length, and the percentage of the popula- tion that dies each year. The importance of these statistics in the fields of game management, basic and applied ecology, and population genetics re- quires no elaboration. The pattern of changing mortality rates with age is best expressed in the form of a life table. These tables usually present the same information in a variety of ways: 1) Survivorship (/x) : this series gives the prob- ability at birth of an individual surviving to any age, x (/x as used here is identical with P, of Leslie, Venables and Venables 1952). The ages 309 Autumn 1966 are most conveniently spaced at regular intervals such that the values refer to survivorship at ages 0, 1, 2 etc. yr, months, or some other convenient interval. The probability at birth of living to birth is obviously unity, but this initial value in the series need not necessarily be set at 1; it is often convenient to multiply it by 1,000 and to increase proportionately the other values in the series. If this is done, survivorship can be redefined as the number of animals in a cohort of 1,000 (or any other number to which the initial value is raised) that survived to each age x. In this way a Rlx series is produced, where k is the constant by which all /, values in the series are multiplied. 2) Mortality (dx) : the fraction of a cohort that dies during the age interval x, x + 1 is designated dx. It can be defined in terms of the individual as the probability at birth of dying during the interval x, x +1. As a means of eliminating decimal points the values are sometimes multiplied by a constant such that the sum of the dx values equals 1,000. The values can be calculated from the /x series by dy =I, — ley 3) Mortality rate (qx): the mortality rate q for the age interval x, x +1 is termed qx. It is calculated as the number of animals in the cohort that died during the interval x, x + 1, divided by the number of animals alive at age x. This value is usually expressed as 1,000qx, the number of animals out of 1,000 alive at age x which died before x + 1. These are three ways of presenting age-specific mortality. Several other methods are available— e.g. survival rate (px), life expectancy (ex) and probability of death (Q,)—but these devices only present in a different way the information already contained in each of the three series previously defined. In this paper only the /x, dx and qx series will be considered. METHODS OF OBTAINING Mortatity DATA Life tables may be constructed from data col- lected in several ways. Direct methods: 1) Recording the ages at death of a large num- ber of animals born at the same time. The fre- quencies of ages at death form a kd, series. 2) Recording the number of animals in the original cohort still alive at various ages. The frequencies from a lx series. Approximate methods: 3) Recording the ages at death of animals marked at birth but whose births were not coeval. The frequencies form a kdx series. MORTALITY PATTERNS IN MAMMALS 907 4) Recording ages at death of a representative sample by ageing carcasses from a population that has assumed a stationary age distribution. Small fluctuations in density will not greatly affect the results if these fluctuations have an average wave length considerably shorter than the period over which the carcasses accumulated. The frequencies form a kdx series. 5) Recording a sample of ages at death from a population with a stationary age distribution, where the specimens were killed by a catastrophic event (avalanche, flood, etc.) that removed and fixed an unbiased sample of ages in a living popu- lation. In some circumstances (outlined later) the age frequencies can be treated as a lx series. 6) The census of ages in a living population, or a sample of it, where the population has assumed a stationary age distribution. Whether the speci- mens are obtained alive by trapping or are killed by unselective shooting, the resultant frequencies are a sample of ages in a living population and form a kil, series in certain circumstances. Methods 1 to 3 are generally used in studies of small mammals while methods 4 to 6 are more commonly used for large mammals. TESTS FOR STATIONARY AGE DISTRIBUTION Five methods have been suggested for deter- mining whether the age structure of a sample is consistent with its having been drawn from a stationary age distribution: a) Comparison of the “mean mortality rate,” calculated from the age distribution of the sample, with the proportion represented by the first age class (Kurtén 1953, p. 51). b) Comparison of the annual female fecundity of a female sample with the sample number multi- plied by the life expectancy at birth, the latter statistic being estimated from the age structure (Quick 1963, p. 210). c) Calculation of instantaneous birth rates and death rates, respectively, from a sample of the population’s age distribution and a sample of ages at death (Hughes 1965). d) Comparison of the age distribution with a prejudged notion of what a stationary age distri- bution should be like (Breakey 1963). e) Examination of the “J,” and “d,’’ series, calculated from the sampled age distribution, for evidence of a common trend (Quick 1963, p. 204). Methods a to c are tautological because they assume the sampled age distribution is either a klx or kd, series; method d assumes the form of the life table, and e makes use of both assumptions. These ways of judging the stationary nature of 310 908 a population are invalid. But I intend something more general than the simple statement that these five methods do not test what they are supposed to test. Given no information other than a single age distribution, it is theoretically impossible to prove that the distribution is from a stationary population unless one begins from the assumption that the population’s survival curve is of a par- ticular form. If such an assumption is made, the life table constructed from the age frequencies provides no more information than was contained in the original premise. MortaALity SAMPLES AND AGE STRUCTURE SAMPLES Methods 4 to 6 for compiling life tables are valid only when the data are drawn from a sta- tionary age distribution. This distribution results when a population does not change in size and where the age structure of the population is con- stant with time. The concept has developed from demographic research on man and is useful for species which, like man, have no seasonally re- stricted period of births. Populations that have a restricted season of births present difficulties of treatment, some of which have been discussed by Leslie and Ranson (1940). Very few mammals breed at the same rate throughout the year, and the stationary age distribution must be redefined if it is to include seasonal breeders. For species with one restricted breeding season each year, a stationary population can be defined as one that does not vary either in numbers or age structure at successive points in time spaced at intervals of 1 yr. The stationary age distribution can then be defined for such popu- lations as the distribution of ages at a given time of the year. Thus there will be an infinite num- ber of different age distributions according to the time of census, other than in the exceptional case of a population having a constant rate of mor- tality throughout life. The distribution of ages in a stationary popula- tion forms a kl, series only when all births for the year occur at an instant of time and the sample is taken at that instant. This is obviously impossible, but the situation is approximated when births occur over a small fraction of the year. If a popu- lation has a restricted season of births, the age structure can be sampled over this period and at the same time the number of live births produced by a hypothetical cohort can be calculated from the number of females either pregnant or suckling young. In this way a set of data closely approxi- mating a kl, series can be obtained. GRAEME CAUGHLEY Ecology, Vol. 47, No.6 If an age distribution is sampled halfway be- tween breeding seasons, it cannot be presented as a klx series with x represented as integral ages in years. With such a sample (making the usual assumptions of stability and lack of bias) neither lx nor dx can be established, but gx values can be calculated for each age interval x + %, x+1¥. The age frequencies from a population with a con- tinuous rate of breeding are exactly analogous; they do not form a kl series but can be treated as a series of the form R (lx + Ix41) /2 This series does not allow calculation of /, values from birth unless the mortality rate between birth and the midpoint of the first age interval is known. Because a sample consists of dead animals, its age frequencies do not necessarily form a mor- tality series. The kdx series is obtained only when the sample represents the frequencies of ages at death in a stationary population. Many published samples treated as if they formed a kdx series are not appropriate to this form of analysis. For instance, if the animals were obtained by shooting which was unselective with respect to age, the sample gives the age structure of the living popu- lation at that time; that the animals were killed to get these data is irrelevant. Hence unbiased shooting samples survivorship, not mortality, and an age structure so obtained can be treated as a kl, series if all other necessary assumptions obtain. Similarly, groups of animals killed by avalanches, fires, or floods—catastrophic events that preserve a sample of the age frequencies of animals during life—do not provide information amenable to kdx treatment. A sample may include both /, and dx compo- nents. For instance, it could consist of a number of dead animals, some of which have been unselec- tively shot, whereas the deaths of others are at- tributable to “natural” mortality. Or it could be formed by a herd of animals killed by an avalanche in an area where carcasses of animals that died “naturally” were also present. In both these cases dx and /, data are confounded and these hetero- geneous samples of ages at death can be treated neither as kdx nor k/x series. Even if a sample of ages at death were not heterogeneous in this sense, it might still give mis- leading information. If, for instance, carcasses attributable to “natural” mortality were collected only on the winter range of a population, the age frequencies of this sample would provide ages at death which reflected the mortality pattern during only part of the year. But the dx series gives the proportion of deaths over contiguous periods of 311 Autumn 1966 the life span and must reflect all mortality during each of these periods. It has been stressed that the frequencies of ages in life or of ages at-death provide life-table in- formation only when they are drawn from a popu- lation with a stationary age distribution. This age distribution should not be confused with the stable distribution. When a population increases at a constant rate and where survivorship and fecun- dity rates are constant, the age distribution even- tually assumes a stable form (Lotka 1907 a, b; Sharpe and Lotka 1911). Slobodkin (1962, p. 49) gives a simple explanation as to why this is so. A stable age distribution does not form a k/x series except when the rate of increase is zero, the season of births is restricted, and the sample is taken at this time. Hence the stationary age distribution is a special case of the stable age distribution. THE RELATIVE USEFULNESS OF THE lx, dx AND Gx SERIES Most published life tables for wild mammals have been constructed either from age frequencies obtained by shooting to give a kl, series, or by de- termining the ages at death of animals found dead, thereby producing a kd, series. Unfortunately, both these methods are almost invariably subject to bias in that the frequency of the first-year class is not representative. Dead immature animals, especially those dying soon after birth, tend to decay faster than the adults, so that they are under- represented in the count of carcasses. The ratio of juveniles to adults in a shot sample is usually biased because the two age classes have different susceptibilities to hunting. With such a bias estab- lished or suspected, the life table is best presented in a form that minimizes this bias. An error in the frequency of the first age class results in dis- tortions of each /, and dy value below it in the series, but gx values are independent of frequencies in younger age classes. By definition, g is the ratio of those dying during an age interval to those alive at the beginning of the interval. At age y the value of q is given by Gy = d;/ly but dy = 1, — Is 44 therefore dy = (ly — ly41) /ly - Thus the value of gy is not directly dependent on absolute values of /, but on the differences between successive values. If the /, series is calculated from age frequencies in which the initial frequency MORTALITY PATTERNS IN MAMMALS 909 is inaccurate, each /, value will be distorted. How- ever, the difference between any two, divided by the first, will remain constant irrespective of the magnitude of error above them in the series. Thus a qx value is independent of all but two survivor- ship age frequencies and can be calculated directly from these frequencies (fx) by Gx ==" Ux — Tae) 1s if the previously discussed conditions are met. The calculation of q from frequencies of ages at death is slightly more complex : dy = df si by definition fee) yal but l, = 2d, — Zd, x=0 <— 0. roo) yo! therefore qy=d,/(2d.—=Zd,) x— 0: D Seal} co = as closely as possible with an adjacent control plot having the same dimensions and vegetative cover. The control plots were open to grazing by rodents, mostly root voles and lemmings. The numbers of flowering plants were counted in three consecutive years. The results are as follows: 1968 1969 1970 Exclosures 61 Wa) 36 Control plots 64 92 33 W093 There were no statistically significant dif- ferences within each year between the flower- ing frequencies of cotton grass in the ex- closures and control plots. On the contrary, 328 8 Ann. Acad. Sci. fenn. Fig. 8. An Eriophorum angustifolium stand examined in the present study. the flowering frequencies in both types of plots varied significantly and synchronously from one year to another. These results indicate that, in our study 4. Variations in quality and Of the results obtained in the previous section, the following three in particular merit further consideration: (1) annual varia- tion and fairly close synchronization of flowering frequency in the two plant species studied; (2) annual variation in the frequency of the youngest vegetative shoots — and youngest rhizomes — in Eriophorum an- gustifolium; (3) annual variation in the frequency of Solidago virgaurea seedlings. 4.1. General With special reference to trees, Lauckhart (1957, p. 232) writes: »Botanists assume that A IV Biologica: — Photo by A. Kaikusalo. area, rodent feeding is not a major cause of annual fluctuations in the flowering of cotton grass. quantity of the rodent food northern plants must manufacture and store food for several years to produce a single seed crop, and when the seed is produced, this crop utilizes all the stored nutrients from the twigs and stems. It seems logical that herbivores feeding on these plants would be influenced by these changes in stor- ed nutrients.» The same applies to many dwarf shrubs and perennial herbs, Solidago virgaurea being an example of the latter. In other perennial plants, such as Frio- phorum angustifolium, the shoot dies after flowering and fruiting, and the growth of the plant continues from new buds. The usual explanation for the death of the shoot 329 JOHAN TAsT & OLAVI KALELA is nutritional: »death is seen as the result of metabolic patterns in which the flowers, fruits and seeds in some way compete so successfully with the rest of the plant for energy sources and other materials that death is the eventual result» (Hillman, 1964, p. 136; cf. Schumacher, 1967, p. 306 ff.). From the point of view of the consumer, it is immaterial to which of these two types its food plants belong. 4.2. Summer food In feeding root voles and lemmings with Eriophorum angustifolium and other species of the sedge family, we used leaves of shoots differing in age but belonging to the same shoot system (see Kalela, 1962). The leaves of the older (e.g. 4-year) shoots were preferred to those of the younger (e.g. 2-year) ones — a result that accords with the above con- clusions based on the principle of an invigor- ation period (cf. p. 2). As a further result of our experiments, all the three green-eaters (Wicrotus oeconomus, Lemmus lemmus and Clethrionomys rufocanus) studied for summer food showed a marked preference for generative plant organs (flower buds, flowers, developing and ripe fruits, moss sporogonia) to vegetative ones (Kalela, 1962). Even in good flowering years, however, the proportion of fertile shoots may be rather small (as was the case in the Eriophorum and Solidago stands studied by us), so it is worth pointing out that the generative organs of widely differing plants were eaten by the experimental animals. In fact, they readily accepted the generative organs (usu- ally excluding the seeds) even of plants be- longing to groups otherwise consumed little, if at all, by them (Kalela, 1962). The above generative plant organs hardly play a major role as an energy source for the rodents in question; of decisive importance are compounds present in these organs which the rodents only need in small amounts. According to Léve & Léve (1945), generative plant organs are generally richer than vegeta- tive organs in substances with estrogenic activity. The biochemical composition of pollens has been extensively studied for apicultural purposes (for a review, see Bar- bier, 1970). The pollens were found to be rich in essential amino acids, vitamins, trace 9 elements and plant-growing substances. In Chauvin’s experiments (1968), a diet con- taining small amounts (1—5 %) of pollen produced a marked increase in birth rates when fed to female mice. Thus when examining, in the next section, the extent to which variations in flowering frequency of a certain food plant are reflected in the fluctuations of rodent numbers, two factors must be borne in mind: (1) the phe- nomenon of »flower-eating», (2) the increase in the nutritional state of the whole plant during the invigoration period that precedes flowering. 4.3. Food from autumn to spring: (a) seeds and seedlings The above is mainly concerned with feed- ing conditions in summer. Passing on to the situation in other seasons, reference may be made first to some studies on certain rodent species known to be seed-eaters by prefer- ence. The unpublished results of experiments carried out by Peiponen indicate that red voles (Clethrionomys rutilus) living in the subalpine region at Kilpisjarvi also have a marked preference for the flowers of herbs and dwarf shrubs. In late summer they change over to seeds, mostly of the same species. A related phenomenon can be seen in the case of red squirrels (Sciurus vulgaris) living in North European spruce forests: in a winter when the spruce bears little seed but plenty of flower buds, the squirrels feed almost exclusively on the latter, concentra- ting on male buds; the following winter they consume the spruce seed (Vartio, 1946; Lam- pio, 1948; Svardson, 1957; Kalela, 1962). In Continental Europe good crops of beechmast and acorns generally give rise to outbreaks of bank vole (Clethrionomys glareolus) (Turéek, 1960). Obviously, assuming that the fructifica- tive rhythm of plants is also reflected in the food conditions of green-eaters in seasons other than summer, the effect must be based on factors other than those mentioned above for seed-eaters. We shall first consider the possible effect of variations in the abundance of seedlings. The stimulating effect of fresh greens on the reproduction of various herbivores has 330 10 Ann. Acad. Sci. fenn. been pointed out by several authors. Recent studies on Microtus montanus (Pinter & Ne- gus, 1965; Negus & Pinter, 1966; Pinter, 1968) have shown that young sprouting shoots of wheat contain hormone-like com- pounds which, even when given in minute quantities, significantly and rapidly stimu- late various parameters in the reproductive physiology of this species. These authors tentatively postulate »plant estrogens» as the agents responsible for such an effect. Similarly, the great abundance of Solidago seedlings as found in our study area in cer- tain springs (e.g. 1970, see p. 7) following profuse flowering is a factor to be considered in examining the spring food conditions of rodents. In Eriophorum angustifolium stands, the amount of fresh greens (sprouting leaves of first-year and older shoots) has also been greater in springs with many new _ shoots (vegetative in this case) than in others. 4.4. Food from autumn to spring: (b) storage organs Vegetative, not generative, propagation is the principal means of reproduction of most of the plants eaten by rodents in our study area. The feeding habits of Microtus oeconomus provide an example of the way in which such plants are used as rodent food in autumn and winter (Tast, 1966; for other species, see IXalela, 1962). Already in August, root voles begin to consume underground organs of certain species of plants. As, among the latter, Eriophorum angustifolium is promi- nent in the area studied by us, attention will be concentrated on it. In the vertical rhizome system of Friopho- rum angustifolilum an individual rhizome, when fully grown or almost fully grown at the onset of its first winter, is generally 20—40 cm long. There is a distinct difference between the shape of first-year rhizomes and that of older ones. The latter are soft, often almost hollow, and dark in colour. The light- coloured first-year rhizomes are compact, due to the abundance of reserve food.} 10n 15th August 120 Eriophorum shoots were dug up and dried at a temperature of 85°C. From this material the weights of first-year and older 331 A IV Biologica: 186 As each rhizome ends in a bud from which a shoot will grow, the amount of first-year rhizomes in winter is reflected by the number of first-year shoots found the following spring. Thus it can be concluded from Fig. 6 that there are sharp annual variations in the amount of the nutrient-rich first-year rhi- zomes of Eriophorum angustifolium. There is little doubt that the winter food resources available to Microtus oeconomus depend to a great extent on this variation, just as the winter food resources available for the seed-eaters depend on the variations in the seed crop. In fact, the spring to spring fluctuations in the numbers of (root) voles clearly parallel the variations in the numbers of first-year rhizomes of the cotton grass (see Figs. 3 and 6). Large quantities of nutrients are obvi- ously required not only for an abundant for- mation of seeds (as in beech and goldenrod) but also for the rich formation of rhizomes of the type found in Friophorum angustifo- lium. First-year rhizomes of the cotton grass have, in fact, been produced most abundantly in years of maximum flowering (1963, 1966 and 1969) or in the summer preceding such a year (1968) — i.e. in years which, according to the principle of an invigoration period, are characterized by a high nutritional state in the plant. A comparable situation was found in the Scotch pine (Pinus silvestris) studied by Hustich (1948, 1956, 1969) in Northern Lapland. The maximum years for growth in the length of annual shoots coincided with maximum intensity of female flowering. Those years were preceded by thermically favourable summers with maximum radial growth. From the above, it can also be understood why, in Eriophorum angustifolium and Solida- go virgaurea with their synchronously varying flowering frequency, there is a co-variation in the amount of first-year shoots in spring, even though they are produced by vegetative means in Eriophorum, and almost exclusively from seedlings in Solidago. Subsections 4.3 and 4.4 give the idea that populations of green-eaters and seed-eaters rhizomes were determined for 10 metres’ rhizome length of each. The dry weight of ‘the first-year rhizomes exceeded that of the older ones by 45 %. JoHAN TastT & OLAVI KALELA do not necessarily differ in principle in their relation to the varying food supplies. The following example illustrates this view. Both in Microtus oeconomus, a green-eater, and in Clethrionomys rutilus, a seed-eater, population growth is probably accelerated in it a summer characterized by profuse flowering of the respective food plants. During the subsequent winter there are plenty of food resources which the increased populations can consume effectively and still survive well. 5. Fluctuations in rodent numbers in relation to food situations, with special reference to Microtus oeconomus Eriophorum angustifolium can be consid- ered the most important food plant of Mic- rotus oeconomus in the study area throughout the year. Solidago virgaurea is also a good example of a plant species used as food by root voles in spring and summer. Therefore, and with reference to the con- clusions drawn in the previous section, there is some justification in simplifying the study of the population fluctuations of Microtus oeconomus in their relation to food situations as follows: (1) The more or less synchronous varia- tion in the flowering frequency of both these plant species will be used as a measure of the nutritional value of the summer food plants of the root vole. (2) The variation in the amount of the young Eriophorum rhizomes will be used as a measure of its winter food resources, bearing in mind, too, the possible significance of the consequent increase of sprouting shoots in spring. (3) The variation in the amount of Solidago seedlings will be used as an additional criterion of the food situation of root voles in spring. Our material on plant production is obviously inadequate to throw light on the fluctuations of the other species of green-eating rodents in the area. But as far as it goes (see p. 2), the effects are simi- lar for the populations of all the species studied. Summer 1963 was characterized by a rich flowering. The following winter the food situation was good. In summer 1964 flower- ing was fairly abundant, though not as much as the previous summer. In 1963 and 1964 the numbers of root voles (and also the total numbers of rodents) grew to a high cyclic level. The subsequent rapid decline took place in winter 1964/1965, during which food was scarce, and continued in summer 1965, which was characterized by a very low flow- ering frequency. The lowest point of the decline was reached in spring 1966. The next good flowering season was sum- mer 1966, which was followed by a winter and spring with fairly good food conditions. Owing to the extremely low level of the initial population in spring 1966, there could be no sharp increase in absolute numbers, though a certain increase could be observed up to spring 1967 (Figs. 1 and 2). In this case, the cyclic increase did not continue; the numbers of rodents dropped between spring 1967 and spring 1968. This is precisely what could be expected according to our hypothesis, be- cause the flowering frequency in summer 1967 was low and the food situation the following winter and spring was poor. Poor flowering continued in summer 1968 but the rich formation of buds for the next winter indicates that invigoration had oc- curred in Eriophorum shoots. The population increase which started that summer continued throughout the next one, leading to a cyclic peak late in 1969. Food conditions were good throughout the winter 1969/70 and continued so the following spring. The populations of most of the rodent species, including Micro- {us oeconomus, were high in spring 1970, but declined rapidly the subsequent summer, when flowering was scanty. The food situa- tion was very poor in winter 1970/71, and in spring and summer 1971 all the rodent popu- lations were extremely low. The above results can be summarized as follows: During the nine years of the study period there were three peaks of flowering frequency with associated peaks in the amount of food in winter and spring. Corresponding to these maxima, there were two distinct highs in the numbers of Microtus oeconomus (and also in the other rodents). The rodent peak corre- 332 12 Ann. Acad. Sci. fenn. sponding to one of the periods of optimum food conditions was abortive owing to the short time (one year) available for the popula- tions to respond to the improving conditions. The clearest correlation between food con- ditions and population fluctuations in rodents occurred in spring.! The abortive peak, too, was visible only in the spring phase. In autumn it levelled out, resulting in a five- year cycle (1964-1969). Such situations pos- sibly account for the fact that five-year cycles are fairly common in the population A IV Biologica: 186 fluctuations of rodents living in Northern Lapland (see Kalela, 1962). The fact that the best correlation between food conditions and population fluctuations is found in spring (when few if any young of the year are included in the catch) stresses the importance of wintering conditions. Ac- cording to the above analysis, however, the size of the spring populations results from a sequence of interconnected food conditions affecting both survival from autumn _ to spring and the reproduction rate in the pre- ceding summer. 6. Synchronizing factors Though the evidence still lies on a narrow basis, the results of this study accord with the view that annual variations in the quality and quantity of the vegetable food are the basic factor responsible for the cyclic nature of the fluctuations in the numbers of rodents in Lapland. On the other hand, there is little doubt that a variety of other factors besides the basic one are at work. These factors, which have to be considered separately in each case, in- clude: (1) over-exploitation of food resources, which accelerates the decline of the popula- tion; (2) stress and its consequences at peak densities; (3) climatic disasters which, direct- ly or by suddenly deteriorating the quality of the food, cut down the number of rodents, regardless of the current population density. Of special interest are the factors that ac- count for the marked synchrony in fluctua- tions characteristic of the northern popula- tion of different rodent species living in the same area. Some of them have been discussed !On comparing the fluctuations in the numbers of rodents at Saananvankka, from where the lon- gest series of annual catches are available (Fig. 3), with year-to-year changes in the numbers of first- year shoots (Figs. 6 and 7) illustrating food con- ditions in spring and previous winter, the following results are obtained: rodents and Eriophorum r = 0.47, rodents and Solidago r = 0.52, and ro- dents and both plant species together R = 0.62; all these figures show positive correlation. 333 in our previous review (IKalela, 1962). The most essential factor was considered to be the shortness of summer in Lapland, owing to which the assimilation periods of plant species tend to coincide, being subject to common fluctuations in climate. Recent studies (see Maher, 1970, and the literature quoted by him) suggest that preda- tion by mustelids plays a marked role in the declining phase of the fluctuations in arctic rodents. Unpublished observations made at Kilpisjarvi by Mr. Jussi Viitala, M.A., in con- nexion with his live-trapping of rodents, support this view. Mustelids (Mustela ermi- nea and M. rixosa) increased rapidly through- out the cyclic rodent high in 1969 and the early summer of 1970. In his trapping area measuring 100 x 200 metres, no less than ten weasels were trapped from 17th July to 3rd August 1970 (the traps were too small for stoats). After June, when the rodent popula- tions had begun to decline, the relative effect of predation by mustelids must have in- creased progressively, contributing effectively to the decline of all the populations, itrespec- tive of species. Acknowledgements. Our best thanks are due to Mr. Simo Lahtinen, M.A. (Institute for Economic Research, Bank of Finland) for his help on sta- tistical problems. This study has been supported by National Research grants from the Council for Sciences. JOHAN TaAsT & OLAVI KALELA 13 References BarRBIER, M. (1970). 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Presented for publication November 12th, 1971 Printed December 1971 335 TERRITORIALITY AND HOME RANGE CONCEPTS AS APPLIED TO MAMMALS By Wiuu1AM Henry Burt TERRITORIALITY The behavioristic trait manifested by a display of property ownership—a defense of certain positions or things—reaches its highest development in the human species. Man considers it his inherent right to own property either as an individual or as a member of a society or both. Further, he is ever ready to protect that property against aggressors, even to the extent at times of sacrificing his own life if necessary. That this behavioristic pattern is not peculiar to man, but is a fundamental characteristic of animals in general, has been shown for diverse animal groups. (For an excellent historical account and summary on territoriality, with fairly complete bibliography, the reader is referred to a paper by Mrs. Nice, 1941). It does not necessarily follow that this trait is found in all animals, nor that it is developed to the same degree in those that are known to possess it, but its wide distribution among the verte- brates (see Evans, L. T., 1938, for reptiles), and even in some of the invertebrates, lends support to the theory that it is a basic characteristic of animals and that the potentialities are there whether the particular animal in question displays the characteristic. Heape (1931, p. 74) went so far as to say: “Thus, although the matter is often an intricate one, and the rights of terri- tory somewhat involved, there can, I think; be no question that territorial rights are established rights amongst the majority of species of animals. There can be no doubt that the desire for acquisition of a definite territorial area, the determination to hold it by fighting if necessary, and the recognition of individual as well as tribal territorial rights by others, are dominant characteristics in all animals. In fact, it may be held that the recognition of territorial rights, one of the most significant attributes of civilization, was not evolved by man, but has ever been an inherent factor in the life history of all animals.” Undoubtedly significant is the fact that the more we study the detailed be- havior of animals, the larger is the list of kinds known to display some sort of territoriality. There have been many definitions to describe the territory of different animals under varying circumstances. The best and simplest of these, in my mind, is by Noble (1939); “territory is any defended area.”’ Noble’s definition may be modified to fit any special case, yet it is all-inclusive and to the point. Territory should not be confused with “home range’”’—an entirely different concept that will be treated more fully later. The territoriality concept is not a new one (see Nice, 1941). It has been only in the last twenty years, however, that it has been developed and brought to the front as an important biological phenomenon in the lower animals. Howard’s book ‘Territory in Bird Life’ (1920) stimulated a large group of workers, chiefly in the field of ornithology, and there has hardly been a bird life-history study since that has not touched on this phase of their behavior. 336 BURT—TERRITORIALITY AND HOME RANGE 347 In the field of mammals, much less critical work has been done, but many of the older naturalists certainly were aware of this behavior pattern even though they did not speak of it in modern terms. Hearne (1795) apparently was thinking of property rights (territoriality) when he wrote about the beaver as ~~ HOME RANGE BOUNDARY BSSSSS) NEUTRAL AREA ----- TERRITORIAL BOUNDARY @ NESTING SITE BLANK--UNOCCUPIED SPACE O REFUGE SITE Fic. 1. Theoretical quadrat with six occupants of the same species and sex, showing territory and home range concepts as presented in text. follows: ‘I have seen a large beaver house built in a small island, that had near a dozen houses under one roof; and, two or three of these only excepted, none of them had any communication with each other but by water. As there were beavers enough to inhabit each apartment, it is more than probable that each family knew its own, and always entered at their own door without having any 337 348 JOURNAL OF MAMMALOGY further connection with their neighbors than a friendly intercourse”’ (in Morgan, 1868, pp. 308-309). Morgan (op. cit., pp. 134-135), also writing of the beaver, made the following observation; ‘‘a beaver family consists of a male and female, and their offspring of the first and second years, or, more properly, under two years old.... When the first litter attains the age of two years, and in the third summer after their birth, they are sent out from the parent lodge.’”? Mor- gan’s observation was later confirmed by Bradt (1938). The works of Seton are replete with instances in the lives of different animals that indicate territorial behavior. In the introduction to his ‘Lives’? Seton (1909) states ‘‘In the idea of a home region is the germ of territorial rights.’”” Heape (1931) devotes an entire chapter to “‘territory.’”’ Although he uses the term more loosely than I propose to, (he includes home ranges of individuals and feeding ranges of tribes or colonies of animals), he carries through his work the idea of defense of an area either by an individual or a group of individuals. Not only this, but he draws heavily on the literature in various fields to support his thesis. Al- though the evidence set forth by Seton, Heape, and other early naturalists is of a general nature, mostly garnered from reports by others, it cannot be brushed aside in a casual manner. The old time naturalists were good observers, and, even though their techniques were not as refined as those of present day biolo- gists, there is much truth in what they wrote. A few fairly recent published observations on specific mammals serve to strengthen many of the general statements made by earlier workers. In speak- ing of the red squirrel (Tamiasciurus), Klugh (1927, p. 28) writes; ‘“The sense of ownership seems to be well developed. Both of the squirrels which have made the maple in my garden their headquarters apparently regarded this tree as their private property, and drove away other squirrels which came into it. It is quite likely that in this case it was not the tree, but the stores that were arranged about it, which they were defending.” Clarke (1939) made similar observations on the same species. In raising wild mice of the genus Peromyscus in the laboratory, Dice (1929, p. 124) found that ‘‘when mice are placed together for mating or to conserve cage space it sometimes happens that fighting takes place, especially at first, and sometimes a mouse is killed.... Nearly always the mouse at home in the cage will attack the presumed intruder.” Further on he states, ‘‘However, when the young are first born, the male, or any other female in the same cage, is driven out of the nest by the mother, who fiercely protects her young.” Similarly, Grange (1932, pp. 4-5) noted that snowshoe hares (Lepus americanus).in captivity ‘‘showed a definite partiality for certain spots and corners to which they became accustomed” and that ‘‘the female would not allow the male in her territory (cage) during late pregnancy and the males themselves were quarrelsome during the breeding season.”’ Errington (1939) has found what he terms “‘intraspecific strife” in wild musk- rats (Ondatra). Much fighting takes place when marshes become overcrowded, especially in fall and winter during readjustment of populations. ‘‘But when invader meets resident in the tunnel system of one of [the] last lodges to be used in a dry marsh, conflict may be indeed savage.”” Gordon (1936) observed def- 338 BURT—TERRITORIALITY AND HOME RANGE 349 inite territories in the western red squirrels (Tamiasciurus fremonti and T. douglasiz) during their food gathering activities. He also performed a neat experiment with marked golden mantled squirrels (C%tellus lateralis chysodetrus) by placing an abundance of food at the home of a female. This food supply attracted others of the same species. To quote Gordon: “she did her best to drive away the others. Some of her sallies were only short, but others were long and tortuous. There were rather definite limits, usually not more than 100 feet from the pile, beyond which she would not extend her pursuit. In spite of the vigor and the number of her chases (one day she made nearly 60 in about 6 hours) she never succeeded in keeping the other animals away.” This individual was overpowered by numbers, but, nevertheless, she was using all her strength to defend her own log pile. To my knowledge, this is the best observation to have been published on territorial behavior in mammals. I have observed a similar situation (Burt, 1940, p. 45) in the east- ern chipmunk (Tamas). An old female was watched fairly closely during two summers. Having marked her, I was certain of her identity. ‘Although other chipmunks often invaded her territory, she invariably drove them away [if she happened to be present at the time]. Her protected area was about fifty yards in radius; beyond this fifty-yard limit around her nesting site she was not concerned. Her foraging range (7.e., home range) was considerably greater than the protected area (territory) and occasionally extended 100 or more yards from her nest site.’”’ From live trapping experiments, plotting the positions of capture of individuals on a map of the area covered, I in- terpreted (op. cit., p. 28) the results to mean that there was territorial be- havior in the white-footed mouse (Peromyscus leucopus), a nocturnal form. When the ranges of the various individuals were plotted on a map, I found that “the area of each of the breeding females is separate—that although areas sometimes adjoin one another, they seldom overlap.”’ Carpenter (1942) writes thus: ‘‘The organized groups of every type of monkey or ape which has been adequately observed in its native habitat, have been found to possess territories and to defend these ranges from all other groups of the same species.” In reporting on his work on the meadow vole (Microtus pennsylvanicus), Blair (1940, pp. 154-155) made the statement ‘It seems evident that there is some factor that tends to make the females occupy ranges that are in part exclusive; .... Possibly there is an antagonism between the females, particularly during the breeding season, but the available evidence does not indicate to me that they have definite territories which they defend against all trespassers. It seems highly probable that most mammalian females attempt to drive away intruders from the close vicinity of their nests containing young, but this does not constitute territoriality in the sense that the term has been used by Howard (1920), Nice (1937), and others in reference to the breeding territories of birds.” (Ital. mine.) To quote Howard (1920, pp. 192-193): “But the Guillemot is generally surrounded by other Guillemots, and the birds are often so densely packed along the ledges that there is scarcely standing room, so it seems, for all of them. Nevertheless the isolation of the individual is, in a sense, Just as 339 350 JOURNAL OF MAMMALOGY complete as that of the individual Bunting, for each one is just as vigilant in resisting intrusion upon its few square feet as the Bunting is in guarding its many square yards, so that the evidence seems to show that that part of the inherited nature which is the basis of the territory is much the same in both species.” Blair, in a later paper (1942, p. 31), writing of Peromyscus manicu- latus gracilis, states: ‘‘The calculated home ranges of all sex and age classes broadly overlapped one another. Thus there was no occupation of exclusive home ranges by breeding females.... That individual woodland deer-mice are highly tolerant of one another is indicated by the foregoing discussion of overlapping home ranges of all sex and age classes.’’ Reporting on an extensive field study of the opossum, Lay (1942, p. 149) states that ‘The ranges of indi- vidual opossums overlapped so frequently that no discernible tendency towards establishment of individual territories could be detected. On the contrary, tracks rarely showed that two or more opossums traveled together.” It seems quite evident that both Blair and Lay are considering the home range as syno- nymous with the territory when in fact they are two quite distinct concepts. Further, there is no concrete evidence in either of the above papers for or against territoriality in the species they studied. It is to be expected that the territory of each and every individual will be trespassed sooner or later regardless of how vigilant the occupant of that territory might be. It is not intended here to give a complete list of works on territorial behavior. The bibliographies in the works cited above lead to a great mass of literature on the subject. The point I wish to emphasice is that nearly all who have critically studied the behavior of wild mammals have found this behavioristic trait inherent in the species with which they worked. Also, it should be stressed, there are two fundamental types of territoriality in mammals—one concerns breeding and rearing of young, the other food and shelter. ‘These two may be further subdivided to fit special cases. Mrs. Nice (1941) gives six major types of territories for birds. Our knowledge of territoriality in mammals is yet too limited, it seems to me, to build an elaborate classification of types. Some day we may catch up with the ornithologists. HOME RANGE The home range concept is, in my opinion, entirely different from, although associated with, the territoriality concept. The two terms have been used so loosely, as synonyms in many instances, that I propose to dwell briefly on them here. My latest Webster’s dictionary (published in 1938), although satisfac- tory in most respects, does not list “home range,”’ so I find no help there. Seton (1909) used the term extensively in his ‘‘Lives’’ where he explains it as follows: “No wild animal roams at random over the country: each has a home region, even if it has not an actual home. The size of this home region corresponds somewhat with the size of the animal. Flesh-eaters as a class have a larger home region than herb-eaters.”” I believe Seton was thinking of the adult animal when he wrote the above. We know that young adolescent animals often do a bit of wandering in search of a home region. During this time they do not have a home, nor, as I consider it, a home range. It is only after they 340 BURT—TERRITORIALITY AND HOME RANGE Soll! establish themselves, normally for the remainder of their lives, unless disturbed,. that one can rightfully speak of the home range. Even then I would restrict: the home range to that area traversed by the individual in its normal activities of food gathering, mating, and caring for young. Occasional sallies outside the area, perhaps exploratory in nature, should not be considered as in part of the home range. The home range need not cover the same area during the life of the individual. Often animals will move from one area to another, thereby abandoning the old home range and setting up a new one. Migratory animals have different home ranges in summer and winter—the migratory route is not considered part of the home range of the animal. The size of the home range may vary with sex, possibly age, and season. Population density also may influence the size of the home range and cause it to coincide more closely with the size of the territory. Home ranges of different individuals may, and do, overlap. This area of overlap is neutral range and does not constitute part of the more restricted territory of animals possessing this attribute. Home ranges are rarely, if ever, in convenient geometric designs. Many home ranges prob- ably are somewhat ameboid in outline, and to connect the outlying points gives a false impression of the actual area covered. Not only that, it may indicate a larger range than really exists. A calculated home range based on trapping records, therefore, is no more than a convenient index to size. Overlapping of home ranges, based on these calculated areas, thus may at times be exaggerated. From trapping records alone, territory may be indicated, if cencentrations of points of capture segregate out, but it cannot be demonstrated without question. If the occupant of an area is in a trap, it is not in a position to defend that area. It is only by direct observation that one can be absolutely certain of terri- toriality. Home range then is the area, usually around a home site, over which the animal normally travels in search of food. Territory is the protected part of the home range, be it the entire home range or only the nest. Every kind of mammal may be said to have a home range, stationary or shifting. Only those that protect some part of the home range, by fighting or agressive gestures, from others of their kind, during some phase of their lives, may be said to have territories. SIGNIFICANCE OF BEHAVIORISTIC STUDIES I think it will be evident that more critical studies in the behavior of wild ani- mals are needed. We are now spending thousands of dollars each year in an attempt to manage some of our wild creatures, especially game species. How can we manage any species until we know its fundamental behavior pattern? What good is there in releasing a thousand animals in an area large enough to support but fifty? Each animal must have so much living room in addition to other essentials of life. The amount of living room may vary somewhat, but for a given species it probably is within certain definable limits. This has all been said before by eminent students of wildlife, but many of us learn only by repetition. May this serve to drive the point home once more. 341 oDZ, JOURNAL OF MAMMALOGY LITERATURE CITED Buarr, W.F. 1940. Home ranges and populations of the meadow vole in southern Michi- gan. Jour. Wildlife Management, vol. 4, pp. 149-161, 1 fig. 1942. Size of home range and notes on the life history of the woodland deer- mouse and eastern chipmunk in northern Michigan. Jour. Mamm., vol. 23, pp. 27-36, 1 fig. Brapt, G. W. 1938. A study of beaver colonies in Michigan. Jour. Mamm., vol. 19, pp. 139-162. Burt, W. H. 1940. Territorial behavior and populations of some small mammals in southern Michigan. Miscl. Publ. Mus. Zool. Univ. Michigan, no. 45, pp. 1-58, 2 pls., 8 figs., 2 maps. CarRPENTER, C. R. 1942. Societies of monkeys and apes. Biological Symposia, Lan- caster: The Jaques Cattell Press, vol. 8, pp. 177-204. CuarkE, C. H. D. 1939. Some notes on hoarding and territorial behavior of the red squirrel Scturus hudsonicus (Erxleben). Canadian Field Nat., vol. 53, no. 3, pp. 42-43. Dice, L. R. 1929. A new laboratory cage for small mammals, with notes on methods of rearing Peromyscus. Jour. Mamm., vol. 10, pp. 116-124, 2 figs. ErrincTon, P. L. 1939. Reactions of muskrat populations to drought. Ecology, vol. 20, pp. 168-186. Evans, L. T. 1938. Cuban field studies on territoriality of the lizard, Anolis sagrei. Jour. Comp. Psych., vol. 25, pp. 97-125, 10 figs. Gorpon, K. 1936. Territorial behavior and social dominance among Sciuridae. Jour. Mamm., vol. 17, pp. 171-172. GrancE, W.B. 1932. Observations on the snowshoe hare, Lepus americanus phaeonotus Allen. Jour. Mamm., vol. 13, pp. 1-19, 2 pls. Hearse, W. 1931. Emigration, migration and nomadism. Cambridge: W. Heffer and Son Ltd., pp. xii + 369. HearNE,S. 1795. A journey from Prince of Wale’s fort in Hudson’s Bay, to the Northern Ocean. London: A. Strahan and T. Cadell, pp. xliv + 458, illustr. Howarp,H.E. 1920. Territoryin birdlife. London: John Murray, pp. xii + 308, illustr. Kuucu, A. B. 1927. Ecology of the red squirrel. Jour. Mamm., vol. 8, pp. 1-382, 5 pls. Lay, D.W. 1942. Ecology of the opossum in eastern Texas. Jour. Mamm., vol. 23, pp. 147-159, 3 figs. Morean, L.H. 1868. The American beaver and his works. Philadelphia: J. B. Lippin- cott and Co., pp. xv + 330, illustr. Nice, M. M. 1941. The role of territory in bird life. Amer. Midl. Nat., vol. 26, pp. 441-487. Nose, G. K. 1939. The role of dominance in the life of birds. Auk, vol. 56, pp. 263-273. Sreron, E. T. 1909. Life-histories of northern animals. An account of the mammals of Manitoba. New York City: Charles Scribner’s Sons, vol. 1, pp. xxx + 673, illustr., vol. 2, pp. xii + 677-1267, illustr. 1929. Lives of game animals, Doubleday, Doran and Co., Inc., 4 vols., illustr. Museum of Zoology, Ann Arbor, Michigan. 342 HIGH ALTITUDE FLIGHTS OF THE FREE-TAILED BAT, TADARIDA BRASILIENSIS, OBSERVED WITH RADAR Trmoruy C. Witiiams, LEONARD C. IRELAND, AND JANET M. WILLIAMS Asstract.—Both search and height-finding radars were used to observe the airborne behavior of free-tailed bats, Tadarida brasiliensis mexicana, near several caves in the southwestern United States. Radar echoes from dense groups of bats covered areas as large as 400 square kilometers and rose to altitudes of more than 3000 meters. The presence of large numbers of bats within these areas was confirmed by visual observation from a helicopter. Bat flights appeared on radar at dusk and at dawn as a slowly expanding or contracting target, usually located near a known roost. The direction in which the echo expanded most rapidly was not due to drift of the bats by winds. This leading edge often moved at more than 40 kilometers per hour, indicating the capacity for rapid, well-directed, high altitude flight in these animals. Bats flying at such high altitudes must employ sensory systems other than echolocation for orientation and navigation. Birds often have been reported flying high above the ground, and recent radar studies of bird migration have revealed that in some cases the majority of migratory birds often may be above 3000 meters (Richardson, 1972; Hilditch et al., 1973). Both the respiratory physiology and the orientational abilities of birds appear especially adapted to high altitude flight (Schmidt-Nielsen, 1971; Griffin, 1969). In contrast, bats usually are considered to be restricted to flight at lower altitudes. One exception is Tadarida brasiliensis mexicana, the free- tailed or guano bat. These bats have been reported flying at high altitudes both at dawn and dusk as they enter or leave their caves in the southwestern United States (Campbell, 1925; Davis et al., 1962; Constantine, 1967a). The exact altitude attained by these small animals is difficult to estimate under crepuscular light conditions, but Davis et al. (1962), using visual triangulation, estimated dawn flights to be as high as 3300 meters. In the present study, ob- servations with radars, employing techniques initially devised for the study of bird migration, were made to gain further information on both the horizontal and vertical distribution of high altitude bat flights near San Antonio, Texas. A helicopter was used to verify the presence of large numbers of bats within radar targets. 807 343 808 JOURNAL OF MAMMALOGY Vol. 54, No. 4 METHODS Three types of radar were used in the present study—search, height-finding, and weather. Three search radars were used to gain information on the horizontal distribution of bats: a 10-centimeter wavelength, 400-kilowatt peak power, ASR-6 approach control radar located at San Antonio International Airport; a 10-centimeter, 100-kilowatt, MPN-14 approach control unit located at Randolph Air Force Base; and a 23-centimeter, 5-megawatt, FPS 91-A surveillance radar located at Lackland Air Force Base. The FPS-6 height-finding radar at Lackland Air Force Base (11-centimeter, 4-megawatt) gave information on the altitude of bat flights. Information concerning both height and horizontal distribution of the bats was obtained from the FPS-77 weather radar at Randolph Air Force Base (5-centimeter, 300-kilowatt). Both the Lackland Air Firce Base height-finder and the FPS-77 weather radar regularly determined the altitude of aircraft to within 200 meters. Although the accuracy for bat targets is not known, there is no reason to suspect an error of more than 200 meters. Further information on these radars may be obtained from the maintenance handbooks published regularly by the Federal Aeronautics Administration (surveillance radars) and the National Oceanic and Atmospheric Administration (weather radar ), both in Washington, D.C. The reader is referred to Eastwood (1967) for an excellent review of the use of radar in orientation research, and to Richardson (1972) for a discussion of the limitations of radars similar to those employed in the present study. Data on horizontal distribution of the bats were recorded from the Plan Position Indi- cator (PPI) of the search radars with either a Polaroid 180 camera or with a time-lapse 8-millimeter camera, which recorded an entire night’s data. Samples of such photographs are shown in Fig. 1. The radars were operated with linear polarization and minimal Sensi- tivity Time Control (STC) to maximize small targets. In most cases, Moving Target Indicator (MTI) was used to reduce ground return from the hills near the bat cave. A discussion of these “anti-clutter” circuits will be found in Richardson (1972). Data on the altitude of bats were recorded from the Range Height Indicator of the height-finding and weather radars with a Polaroid camera (Fig. 2), or by visual inspection of the display when the camera was not available. No “anti-clutter” circuits were used on the height-finding radars. Observations were made from 20 to 29 October 1967, 6 June to 1] August 1968, and 19 July to 26 August 1971. Observations were made on a non-interference basis and, thus, other operations at the radar sites often prevented our obtaining continuous coverage of bat activity. Whenever possible, observations were started at least 1 hour before sunset or sunrise and continued for as long as bat activity was discernible on the radar displays. All radars used in this study were subject to night-to-night changes in sensitivity due to changed atmospheric conditions or maintenance adjustments of the radars. At present we do not know the degree to which these sensitivity changes affect the size and shape > Fic. 1—PPI photograph of bats emerging from several caves near San Antonio, Texas. Photographs are of the Lackland AFB FPS-91-A PPI with MTI. True compass bearings from the radar are indicated at the periphery of the display. Photographs were taken on 10 August 1968, A at 2045 hours, B at 2105 hours, and C at 2122 hours Central Daylight Savings Time. Ring at about one-fourth radius of lower figure is 32 kilometers range from the radar. White arrows in upper figure point to the location of known bat roosts: Frio (F), Val Verde (V), Nye (N) and Bracken (B), given in Davis et al. (1962), and a deserted railroad tunnel (R), described in Constantine (1967b). Note large targets in lower figures appear near these large roosts. 344 November 1973 WILLIAMS ET AL.—FLIGHTS OF TADARIDA 210 200 190 189 170 st 345 809 810 JOURNAL OF MAMMALOGY Vol. 54, No. 4 of the radar echoes seen on the PPI and RHI displays. For this reason, we have avoided comparing data on magnitude of bat targets from different radars or on different nights, and measurements of magnitude of radar echoes should be taken as minimum values. Direction, speed, and altitude data appeared to be less affected by changes in radar sensitivity. Observations from a Helicopter Visual observation from a helicopter was used to verify the presence of bats within the targets seen on radar. We used a small twin rotor fire rescue helicopter equipped with floodlights for this purpose. Bats could be reliably identified if they passed through a cylindrical area roughly 30 meters long and 15 meters in diameter, extending downward from the aircraft at about 45 degrees. Such observations were possible only if the airspeed of the helicopter was kept below 60 kilometers per hour. It was not possible to reliably count more than 30 animals per minute passing through the searchlight. Weather Observations Hourly surface weather observations were obtained from the 24th Weather Squadron at Randolph Air Force Base, located 17 kilometers south-southeast of Bracken Cave. No winds aloft data were available from the San Antonio area. Winds were, therefore, extrapolated from winds aloft data obtained from radiosondes at Victoria, Texas (160 kilometers south- east of Bracken Cave), and Midland, Texas (460 kilometers northwest of the cave). These stations made observations at 0000 and 1200 Greenwich Mean Time (0700 and 1900 hours local time). Personnel at the local weather bureau in San Antonio informed us that this technique should give winds aloft to within 20 degrees at San Antonio for windspeeds greater than 10 kilometers per hour. RESULTS Typical Appearance and Development of Bat Targets on Radar Radar observations of Bracken Cave were made on 51 occasions, and ap- proximately 3 hours of radar data were collected during each observation period. Thirty-five observation periods were conducted during the evening and 16 in the morning. Information from both search and _height-finding radars was obtained on 14 occasions, exclusively from search radars on 26, and from height-finders alone on three. Bat targets were not observed on eight occasions due to heavy rainstorm in the area (see below). Fig. 1 shows a series of photographs taken of the Lackland Air Force Base search radar PPI and illustrates the typical horizontal development of radar echoes that represent the emergence of bats from several large caves. The white arrows in Fig. 1A indicate the position of five large bat roosts, including Bracken Cave, reported by Davis et al. (1962), and by Constantine (1967b). This photograph was taken 20 minutes after sunset. At this time observers at Bracken Cave reported that a column of bats had emerged from the cave, attained an altitude of at least 150 meters, and was not less than 1.5 kilometers long. Note that small irregular targets can be seen near the roosts; the larger circular echoes, which were moving rapidly, represent aircraft. Fig. 1B shows the appearance of the same radar display 20 minutes later. The bat echoes have now expanded and assumed a fan-shaped form. Of the 164 bat radar targets we recorded, including those near roosts other than 346 811 WILLIAMS ET AL.—FLIGHTS OF TADARIDA November 1973 = & ® .S) SS) ™~ = I fe) 5 10 15 20 25 Frange (km) a a S a) vo 3 oN = sg e) 5 10 18 20 25 Frange (km) b Photographs of Fic. 2.—Altitudinal distribution of bats emerging from Bracken Cave. A, taken at the RHI display (see text) of the FPS-77 at Randolph Air Force Base, Texas. 2110 hours Central Daylight Savings Time, shows the pattern of ground echoes in the area. The bats are the small mound rising toward the tip of the white arrow. The two vertical lines are range marks in the RHI display. B, taken at 2125 hours (CDST), illustrates the development of a layer of bats (white arrow) leaving the cave. Altitude in meters above sea level is given at left; subtract about 300 meters to obtain altitude above ground level. Range of target from the radar is given at bottom of each figure. 347 812 JOURNAL OF MAMMALOGY Vol. 54, No. 4 Bracken, 152, or 98 per cent, showed a rough fan shape at some time during their development. In some cases a bat echo expanded relatively rapidly in only one direction, in other cases the echoes expanded in two separate direc- tions, possibly indicating two flight directions. At the time Fig. 1B was taken, observers at the Bracken Cave reported that the column of bats extended as far (more than 1.5 kilometers) and as high (about 300 meters) as they could see in the dim light. Also, in Fig. 1B numerous small targets may be seen developing to the southeast of the radar. These targets followed the same pattern of development as did larger targets, remaining essentially stationary and slowly expanding, probably indicating the location of a large number of relatively small bat roosts. The bat targets continued to expand until they reached the size indicated in Fig. 1C, about an hour after sunset. They then gradually grew more diffuse until it appeared that a fine clutter covered almost the entire PPI screen. This diffuse activity often remained visible for 1 to 2 hours. Both circumstantial and direct evidence indicated that these large radar echoes were due to bats. Such echoes are seen only during months when large numbers of T. b. mexicana are resident in the area, only at sunrise and sunset, and reliably only near large active bat roosts. The presence of bats in these large formations was confirmed by visual observation from a helicopter (see below). Fig. 2 shows two photographs of the RHI display of the FPS-77 weather radar used in the height-finding mode with the radar beam directed toward Bracken Cave. These pictures illustrate the typical vertical dispersion of bat echoes. Bats emerging from the cave were first seen (Fig. 2A) as a small mound rising above the clutter due to ground return. In Fig. 2B, taken 15 minutes later, the column has risen to a height of about 3000 meters and has progressed about 9 kilometers toward the radar. The increased return near the ground in Fig. 2B probably represents low-flying bats. Data from height- finding radars repeatedly indicated that the bats were distributed as a layer approximately 350 to 500 meters thick and extending outward from the cave. Greater detail than is shown in Fig. 1 was gained by decreasing the total area covered in a PPI display and observing the emergence from a single roost. Repeated visual inspection of the PPI and time-lapse movie films showed that the large targets, such as shown in Fig. 2, were actually made up of many smaller targets that we will term sub-targets. These sub-targets appeared near the location of the bat roost, then moved outward through the length of the large target and diminished and disappeared at its periphery. Within the large targets, the impression was of an ever changing mass of scintillating luminous dots similar in appearance to large scale passerine bird migrations viewed on radar (Drury and Nisbet, 1964), but confined to a discrete area. Due to the large numbers of these sub-targets and their scin- tillating nature, it was not possible to measure the exact speed of any single sub-target. But in all cases the majority of sub-targets moved toward those 348 November 1973 WILLIAMS ET AL.—FLIGHTS OF TADARIDA 813 areas in which the large radar target was expanding most rapidly, although sub-targets could be seen leaving the main target at all points of the compass. During morning activity, the sequence of events shown in Figs. 1 and 2 occurred in reverse order. One to 2 hours before sunrise, small scintillating targets would appear in the vicinity of bat roosts. These would increase in number until they formed radar targets similar to those in Fig. 1B. Over the next 1 to 3 hours the morning targets would slowly diminish in size, dis- appearing usually about 1 hour after sunrise. The small scintillating targets were similar to those described above but appeared near the edge of the large targets and moved toward the approximate position of the cave. The fanlike shape of the targets seen in the morning indicates that the bats tend to enter their roosts nonrandomly, with the major portion of the bat flight approaching the cave from a single direction. The succession of events shown in Fig. 1 indicates the general pattern of development of bat echoes. Exceptions to this general pattern occurred on four occasions when two separate flights of bats were seen to emerge from a single cave, with intervals of from 20 to 60 minutes between flights. All observations during 1967 and 1968 were made in clear, or partially overcast weather when no rain was present in the area. Unusually heavy rainfall occurred in the study area during the summer of 1971. Radar observations made during rain revealed greatly reduced bat activity; heavy rainstorms were in the area on the eight occasions when bats failed to produce echoes near Bracken Cave. At this time circular polarization (CP) (see under Methods above) was often used to reduce the returns from rain clouds. Tests with CP at other times showed that this circuit reduced the size of a bat target on the PPI display by approximately 30 per cent. Because no targets at all were seen during the inclement weather mentioned above, it is unlikely that large numbers of bats emerged from Bracken Cave at that time. Observations from a Helicopter fhe presence of large numbers of bats within the areas indicated by the radar targets was verified by direct visual observation from a_ helicopter equipped with floodlights. On two evenings the aircraft was directed to fly across the large radar target near Bracken Cave. Within the radar target large numbers of bats would suddenly flash through the light beam more rapidly than the observer could count (more than 30 per minute) and then disappear, followed rapidly by another group. Beyond the perimeter of the radar targets, bats were far less numerous and were flying singly or in groups of less than 10. The greatest concentration of animals outside the radar targets was usually within 160 meters of the ground and these bats were often observed flying with the characteristic darting flight of feeding animals. These feeding flights were not seen in bats above 200 meters. Insects upon which the bats feed were common at less than 200 meters, passing like rain through the beam of the searchlights, but were rarely seen above 200 meters. 349 814 JOURNAL OF MAMMALOGY Vol. 54, No. 4 TABLE 1.—Number of Tadarida brasiliensis mexicana seen from a helicopter at night in a 2-minute interval. Altitude Counts made Counts made above ground inside radar outside level (meters ) target radar target 1500-1330 1 i 1300-1160 i 2 1160-1000 3 4 1000-830 8 i 830-660 13-+ 1 660-490 26-+ 1 490-320 8 z 320-160 si 2 160-0 is 15+ * 300 meters was the minimum altitude for night flight in this area. Further data on the flight patterns of bats leaving Bracken Cave was gained by observing the bat flight from the helicopter before sunset. The aircraft was positioned about | kilometer west of the column of emerging bats at an altitude of approximately 330 meters. The thick column of bats that emerged from the cave first broke up into large groups of 10,000 to 1000 animals; these in turn divided into groups of 1000 to 100. These small groups may well have formed the small scintillating sub-targets seen to move across the large bat echoes on the search radar PPI displays. Presumably these small groups con- tinued to disperse until, near the edge of the large radar echoes, they diminished below the critical density for detection by radar. Thus, it appears that the large targets seen by radar were due to reflection of radar energy from groups of more than 100 animals flying in close proximity. The existence of such concentrations of small animals would explain the ability of radar to detect bats at ranges of up to 150 kilometers. The vertical distribution of bats was investigated by moving the helicopter up or down in a spiral both within and outside the radar targets near Bracken Cave. Observations were restricted to less than 1500 meters above ground level. The most extensive probes were made between 2000 and 2200 hours (local time) on the night of 8 August 1965. Data from the two probes on this date, one inside the radar target, are listed in Table 1. The bats observed within the radar target were concentrated in a layer between 800 and 500 meters altitude. The slight increase in numbers of bats beyond the radar target at altitudes of 1000 to 1300 meters may indicate a continuation of the layer seen close to the cave but with the bats too widely dispersed to produce a radar echo. On the same night, height-finding radar indicated that the bat flight was less than 1000 meters above the ground. Incomplete separation of bat targets from ground return prevented accurate altitude measurement. A similar situation may be seen in Fig. 2B; a flight of bats below the high altitude flight blends into the ground return. 350 November 1973 WILLIAMS ET AL.—FLIGHTS OF TADARIDA 815 TABLE 2.—Radar observations of bat targets (Tadarida_ brasiliensis mexicana) near Bracken Cave, Texas. Maximun rate of climb Maximum Maximum Maximum (meters Direction extent speed (km altitude / per Date Radar of flight (km ) per hour) Radar minute ) Evening Activity 1968 (Als: A NNE 15 36 2400/HL 93 7/14 A NNW 10 33 2900/HL 70 7/18 A S 10 15 2600/HL 60 7/24 WwW NE 10 100 2000/W 10 oul WwW NE 25 80 2900/W 8 8/1 A NE 5) 27 2700/HL 120 8/5 L N 25 25 2100/HL 50 8/9 R NW-+NE a 19 3100/W 100 8/11 W E 12 45 2100/W 50 1971 es L WNW 9 105 1550/W 9 Morning Activity 1968 7/20 A SW 8 — 1300/HL — 8/2 A NNE 10 ~- 3000/HL — 8/3 A N 5 —— 3000/HL —— 8/4 A N 12 — 2500/HL — Radar identification code: A — ASR-6 at San Antonio International Airport, L = FPS-91-A at Lackland Air Force Base, R= MPN 14 at Randolph Air Force Base, HL =FPS-6 at Lackland Air Force Base, W = FPS-77 at Randolph Air Force Base. Variations in Bat Targets Bat targets varied in size, direction of motion, speed of the leading edge, altitude, and rate of climb. Although bat emergence patterns from several caves were observed on the four nights we used the long range Lackland Air Force Base radar (see Fig. 1), the greater majority of our observations were made of the Bracken Cave, and, thus, the following analyses pertain only to that roost. Data obtained on all occasions when it was possible to obtain simultaneous search and height finding radar information are listed in Table 2. As discussed under Methods above, great care must be exercised in com- paring data on size and density of radar targets due to large variations in radar sensitivity. Direction—F light direction, as listed in Table 2, was taken as the direction of the principal axis of the radar target from the cave for evening observations, and toward the cave for morning observations. Flight directions from Bracken Cave recorded during all evening observation periods are shown in Fig. 3. Bat targets leaving this roost were photographed on 28 occasions; on four evenings 351 816 JOURNAL OF MAMMALOGY Vol. 54, No. 4 dj oo@6ceee|- Fic. 3.—Flight directions taken by bats emerging from Bracken Cave, as shown on radar. Closed circles indicate that MTI was in use when flight direction was determined. Open circles indicate normal radar. Closed arrows show the area of expected maximum MTI suppression of targets for both the Lackland AFB FPS-91-A and the San Antonio Airport ASR-6 (because the two radars are located along a straight line joining them to Bracken Cave, areas of expected maximum suppression are the same for both units). Open arrows show the area of expected minimum suppression. two separate flight directions were recorded, giving a total of 36 data points in Fig. 3. There did not appear to be any single preferred flight direction for exit from Bracken. A Chi-square test for goodness of fit (Batschelet, 1965) applied to this distribution of flight directions, however, indicated that the distribution was not uniform (x7, = 15.33, df =5, P < .01). There appears to be a clustering of data points both to the northeast and to the southwest of the cave. This clustering was probably influenced by MTI circuitry, which tends to accentuate targets moving toward or away from the radar. The axes of expected maximum and minimum suppression are shown in Fig. 3. MTI circuitry was not, however, the sole determining factor of our observed flight directions. Most flight directions recorded on normal radar, when MTI was not in use, were included in the two clusters of data points to the northeast and to the southwest of the cave. A Chi-square test applied to the distribu- tion of flight directions recorded when MTI was in use, with four groups, defined as a 90-degree sector of the unit circle bisected by either a line of maximum or minimum suppression, was not significant (x, = 4.33, df =3, 302 November 1973 WILLIAMS ET AL.—FLIGHTS OF TADARIDA 817 P > .05). The hypothesis that the distribution was uniform, therefore, could not be rejected on the basis of this sample. The dispersal of bats from their caves in one or two principal directions might be due either to drift by winds aloft or to active flight in a preferred direction. The average difference between wind direction and flight direction for bats leaving the cave was 57 degrees, when all flight directions deter- mined by search radar were considered and the wind direction was taken as that at 1500 meters. If we repeat the computations using only the nine cases of bats leaving the cave for which flight direction, altitude, and winds at that altitude are known (Table 2), the value is 68 degrees. Thus, it appears that the flight directions seen on radar are not simply due to wind drift of an ascending column of bats but reflect some degree of horizontal flight in a preferred direction. The mean difference as calculated above for all bat flights returning to their roosts was 88 degrees, and for only those listed in Table 2 is 103 degrees. This indicates that at least in the final approach to their caves bats do not tend to fly either upwind or downwind. Size of target—As mentioned above, under Methods, changes in radar sensitivity produce probably small, but at present unknown, variations in the size of bat echoes on a PPI display and, thus, we cannot compare data from different radars or data from different nights in detail. The following limited analyses, however, appear warranted. Bat radar targets recorded from all roosts, including those shown in Fig. 1, varied from 5 to 25 kilometers in length and from 20 square kilometers to over 400 square kilometers in area. The mean length for evening activity was 17 kilometers with a standard devia- tion of 7 kilometers and for morning activity was 9 kilometers (standard deviation, 3 kilometers). These variations might reflect true differences in numbers or flow patterns of bats emerging from a cave (Herreid and Davis, 1966), or they might result from differential sensitivity of radars to bat flights at various altitudes. The correlation between length of echo and altitude for the observations in Table 2 was + .24 (P>.05). The lack of a significant correlation between these two parameters indicates that altitude is not a major factor in the size of a target seen on the PPI display once a flight of bats rises into the radar beam. Thus, variations in the size of radar targets probably reflect variations in the numbers of bats aloft. Speed.—An estimate of the horizontal flight speed of bats was gained by measuring the maximum rate of expansion over intervals of 5 to 10 minutes of the large targets on each night. The speed of the small scintillating targets mentioned above was in most cases greater than the expansion of the whole target. The speed of the leading edge of the bat targets emerging from Bracken Cave (measured over at least 5 kilometers) ranged from 7 to 105 kilometers per hour, with a mean of 40 and a standard deviation of 25 kilometers per hour (see also Table 2). 353 818 JOURNAL OF MAMMALOGY Vol. 54, No. 4 Some of the higher speeds recorded might be due to bats flying lower than the radar horizon for a period of time and then ascending, producing a sudden expansion of the radar echo. The majority of these observations are, however, lower than the maximum flight speed of 100 kilometers per hour for T. b. mexicana as estimated by Davis et al. (1962). Horizontal speed was negatively correlated with rate of climb. Rates of climb varied from 7 to 120 meters per minute, with a mean of 57 and a standard deviation of 40. The correlation between speed of the leading edge and rate of climb for the nine cases where both measures were available (Table 2) was -—.85 (P< .01). This indicates, as would be expected, that bats displaying a high vertical velocity have a low horizontal velocity, and suggests that only our highest speeds represent bats in level flight. Altitude.—For our calculations of the altitude of bat flights, we used the top of the major echo shown on the RHI display (Fig. 2). The majority of bats would be flying below this level, but a few small targets, presumably small groups of bats, were often found up to 500 meters above this level. During the course of four morning and 13 evening observation periods, the average maximum altitude reached by bat flights was 2300 meters (standard devia- tion, 600 meters), and the range was from 600 meters to 3100 meters above ground level. Approximate altitude above sea level may be obtained by adding 300 meters to these figures. Thus, high altitude flights appear to be common for T. b. mexicana both when entering and when leaving their roosts. DISCUSSION Radar has revealed that free-tail bats appear to leave and return to large roosts in massive high altitude formations, which may extend over an area greater than 400 square kilometers and rise to altitudes of more than 3000 meters. These formations are not constant from night to night, but change in both altitude and horizontal distribution. The speed of the leading edge of bat radar targets, the fact that the direction of motion of the leading edge does not appear to be due to prevailing winds, and the orientation of the majority of the small, relatively faster targets within the main target toward the leading edge, argues against an entirely random pattern of dispersion by T. b. mexicana, and for the conclusion that these bats make rapid, well- directed and perhaps goal-oriented flights. The flight patterns of these bats are remarkable for both their large hori- zontal extent and their altitude. Both rapid sustained horizontal flight and flight at altitudes of 3 kilometers suggests that bats may be capable of the high, long-distance flights shown by many species of birds during migration (see Eastwood, 1967). This conclusion is supported by studies with Myotis lucifugus, which have revealed homing speeds of 32 kilometers per hour (Mueller, 1966), and by banding studies that have shown T. b. mexicana makes yearly migratory flights of 1300 kilometers (Constantine, 1967a). The reader is referred to Griffin (1970) for a review of bat homing and migration. 304 November 1973 WILLIAMS ET AL.—FLIGHTS OF TADARIDA 819 Physiological adaptations for high altitude flight in bats are at present un- known. Experiments by Thomas and Suthers (1973) have revealed that the average oxygen consumption of flying bats is similar to values obtained for birds by Tucker (1968), but bats lack air sacs and other adaptions believed important for high altitude flight of birds (Bretz and Schmidt-Nielsen, 1971; Schmidt-Nielsen, 1971). The known orientation systems of bats appear inadequate for guidance at altitudes of 3000 meters. Olfaction and audition appear to operate only at short range (Twente, 1955). Griffin (1971) has shown that echolocation is restricted to a range of less than 300 meters. Wieder-orientierung, or spatial memory (Mohres and Oettingen-Spielberg, 1949; Neuweiler and Mohres, 1967) appears restricted to orientation within a fixed and probably learned path rather than for paths that change from night to night. Vision was shown to be used for homing of Phyllostomus hastatus by Williams et al. (1966) and Williams and Williams (1970), and this may be the sense used by T. b. mexicana. However, in the absence of large landmarks such as mountains or coastlines, visual piloting might prove difficult for animals with the limited visual acuity of bats (Suthers, 1966). The stars might also be used to obtain directional information as has been shown for birds by Sauer and Sauer (1960) and Emlen (1967). During our studies it was not possible to observe the airborne behavior of bats under totally overcast skies. Thus, the use of either the stars or sunset and sunrise for orientation remains a real but untested possibility. Finally, we must acknowledge that there may be some as yet unknown sensory system used by bats for orientation. Observations of birds maintaining course without being able to see either the sky or the earth indicate that we have yet to understand the total sensory information available to flying ani- mals ( Bellrose, 1967; Griffin, 1969; Williams et al., 1972). The advantages of high altitude flights to bats are at present unclear. Tadarida brasiliensis did not appear to be feeding, and although Gressitt and Yashimoto (1963) reported finding insects at altitudes up to 5700 meters above the Pacific Ocean, our observations from a helicopter revealed few insects above 500 meters. Davis et al. (1962) suggested that T. b. mexicana may fly 100 kilometers or more in their nightly feeding flights. If bats were able to obtain tailwinds at high altitudes, the effort expended in reaching these altitudes might be offset by the reduced effort required for long distance flight. At present we lack sufficient physiological data for such calculations, and our data are insufficient to test whether the bats tended to choose the most favorable altitude for a given flight direction. ACKNOWLEDGMENTS We are deeply indebted to the many men of the United States Air Force and the Federal Aviation Administration who assisted us in this research. Funds were provided by the United States Air Force Office of Scientific Research through a contract with the Office 355 820 JOURNAL OF MAMMALOGY Vol. 54, No. 4 of Ecology, Smithsonian Institution, H. Buechner, Head, and through grant no. AFSOR- 71-2123 to the Research Foundation of the State University of New York. Analysis of the data was also accomplished under National Science Foundation grants GZ-259 and GB- 13246 to the Woods Hole Oceanographic Institution. We are indebted to Dr. D. R. Griffin and to Dr. C. H. Herreid for their helpful suggestions on the manuscript. LITERATURE CITED BATSCHELET, E. 1965. Statistical methods for the analysis of problems in animal orienta- tion and certain biological rhythms. AIBS, Washington, D.C., 57 pp. BELLROSE, F. 1967. Radar in orientation research. Proc. 14th Omith. Cong., Blackwell, Oxford, pp. 281-309. Bretz, W. L., AND K. ScumMipt-NiELsEN. 1971. Bird respiration: Flow patterns in the duck lung. J. Exp. Biol., 54:103-118. CaMPBELL, C. A. R. 1925. Bats, mosquitoes and dollars. Stratford, Boston, 262 pp. ConsTANTINE, D. G. 1967a. Activity patterns of the Mexican free-tailed bat. Univ. New Mexico Press, Publ. Biol., 7: 1-79. 1967b. Rabies transmission by air in bat caves. Publ. U.S. Public Health Serv., 1617:ix + 1-51. Davis, R. B., C. F. Herrem II, anno H. L. Suorr. 1962. Mexican free-tailed bats in Texas. Ecol. Monogr., 32:311-346. Drury, W. H., ANd I. C. T. Nisper. 1964. Radar studies of orientation of songbird migrants in southeastern New England. Bird Banding, 35:69-119. Eastwoop, E. 1967. Radar ornithology. Methuen and Co., London, 278 pp. EMLEN, S. 1967. Migratory orientation in the Indigo bunting Passerina cyanea. Parts I and II. Auk, 84:309-342 and 463-489. GressiTT, J. L., AND C. M. YAsHtMoro. 1963. Dispersal of animals in the Pacific. Proc. 10th Pacific Sci. Cong., Bishop Mus. Press, Honolulu, Hawaii, pp. 283-292. GrirFIn, D. R. 1969. The physiology and geophysics of bird navigation. Quart. Rev. Biol., 44;:255-275. — —. 1970. Migrations and homing of bats. Pp. 233-264, in Biology of Bats (W. A. Wimsatt ed.), Academic Press, New York, 1:xii + 1-406. 1971. The importance of atmospheric attenuation for the echolocation of bats (Chiroptera). Anim. Behav., 19:55-61. Herreiw, C. H., ano R. B. Davis. 1966. Flight patterns of bats. J. Mamm., 47:78—86. Hinpircn, C. D. M., T. C. WitxiaMs, AND I. C. T. Nisper. 1973. Autumnal bird migra- tion over Antigua, W. I. Bird Banding, 44:171-179. Moures, F. P., AND T. OETTINGEN-SPIELBERG. 1949. Versuche uber die Nahorientierung und das Heimfindevermogen der Fledermaiise. Verhandlung der Deutschen Zoologen in Mainz, pp. 248-252. MvuELLeR, H. 1966. Homing and distance orientation in bats. Z. Tierpsychol., 23: 403-421. NEUWEILER, G., AND F. P. Moures. 1967. Die Rolle des Ortsgedichnisses bei der Orientierung der Grossblatt Fledermaiise, Megaderma lyra. Z. Vergl. Physiol. NEE WAy RicHarpson, J. 1972. Temporal variations in the ability of individual radars in detecting birds. Field notes Associate Committee on Bird Hazard to Aircraft, Nat. Res. Council, Ottawa, Canada, 61:1-58. SAvuER, E. G. F., Ano E. M. Saver. 1960. Star navigation of nocturnal birds. Cold Springs Harbor Symp. Quant. Biol., 25:389-393. SCHMIDT-NIELSEN, Kk. 1971. How birds breathe. Sci. Amer., 225:72-88. SuTHERS, R. 1966. Optomotor responses by echolocating bats. Science, 152:1102-1104. 306 November 1973 WILLIAMS ET AL.—FLIGHTS OF TADARIDA 821 Tuomas, S. P., AND R. A. SurHers. 1973. The physiology and energetics of bat flight. J. Exp. Biol., in press. Tucker, V. A. 1968. Respiratory exchange and evaporative water loss in the flying Budgerigar. J. Exp. Biol., 48:67—87. Twente, J. W. 1955. Aspects of a population study of cavern-dwelling bats. J. Mamm., 36:379-390. WituraMs, T. C., Ano J. M. WitiiaMs. 1970. Radio tracking of homing and feeding flights of a neotropical bat Phyllostomus hastatus. Anim. Behav., 18:302-309. WituiAMs, T. C., J. M. WitiiaMs, AND D. R. GrirFin. 1966. The homing ability of the neotropical bat Phyllostomus hastatus, with evidence for visual orientation. Anim. Behav., 14:468—473. WixuiaMs, T. C., J. M. Wituiams, J. M. TEAL, AND J. W. KANisHER. 1972. Tracking radar studies of bird migration. Animal orientation and navigation: a sym- posium, NASA SP-262, Washington, D.C. Department of Biology, State University of New York, Buffalo (present address of Ireland: Department of Psychology, Oakland University, Rochester, Michigan). Accepted 20 February 1973. 357 EFFECT OF HABITAT QUALITY ON DISTRIBUTIONS OF THREE SYMPATRIC SPECIES OF DESERT RODENTS Heteromyid rodents Dipodomys deserti Stephens, Dipodomys merriami Mearns, and Perognathus longimembris (Coues) coexist in the Kelso Dune area, Mojave Desert, San Bernardino County, California. During summer 1970 these rodent species were trapped in adjacent dune and valley habitats during two periods of differing habitat quality. During the first or “before” time period (1 July to 15 August), habitat conditions were very poor due to a continuing local drought. Evidence supporting this judgement on habitat quality follows. I observed no annual plant growth or perennial seeding during visits to the area during winter and spring of 1969 to 1970; none of the rodents captured during the summer were reproductively active and none were juveniles. The “after” period occurred when the drought was temporarily broken on 15 August. An intense cloudburst drenched the area resulting in a period of rapid growth and flowering of first annual and then perennial plants. This paper compares distributions of the three rodent species in dune and valley habitats and changes in their distribution from “before” to “after” periods. This comparison provides insight into mechanisms of habitat selection and spatial separation of these species. Field data on species dominance were obtained by baiting an area with wild bird seed to maximize rodent densities. Observations were then made on interspecific encounters from a platform using battery-powered red lights for illumination. In 11 interspecific encounters between kangaroo rats, D. merriami would retreat from the larger D. deserti. Retreat always began before any physical contact took place and the dominant individual showed little or no interest in pursuit. In four encounters with either of the kangaroo rat species, P. longimembris always retreated with no interest in pursuit being shown by the kangaroo rats. Individuals of each species were trapped and exposed to each other in the laboratory to gather supportive evidence on species dominance. Each encounter took place during early evening in a 1.0 by 1.8 meter (m) cage illuminated by a dim red light and center divided with plywood. A single individual of each of two species was placed in opposite ends of the divided cage and allowed five minutes to adjust before the divider was removed. All actions and postures were noted for ten minutes, or less if fighting seriously endangered one of the individuals. Five trials of each of the four combinations of species were tested. Both field and laboratory observations showed that D. deserti was by far the most aggressive species and the dominant rodent. D. merriami, the subordinate kangaroo rat, was dominant in all encounters with P. longimembris. Results of these observations were used to supplement distribution data obtained from the trap grid. 308 660 JOURNAL OF MAMMALOGY Vol. 55, No. 3 TABLE 1.—Summary of recapture frequencies and total captures of three rodent species during summer 1970. Species Recapture Frequencies D. deserti D. merriami P. longimembris 1 7 3 10 2 to 5 +) r) 8 6 to 10 l 3 aL 11 to 15 2 0) 0 Total number of individuals (N) > ) 19 Total captures 61 oy 39 A study plot was selected in an area where there was a sharp boundary between dune and valley habitats. A four hectare trapping grid consisting of 140 trap stations with 18 m between stations was placed half on dunes and half on valley floor. A single Sherman live trap was placed at each station and baited with wild bird seed and peanut butter. Dune and valley were trapped with a roving, alternating trap row procedure to help prevent rodents from becoming trap “shy” or trap “bums.” Each trap was set late in the evening, checked and sprung before 0800 to prevent heat death of any captives. The area was trapped continuously from July through August 1970. Forty-three rodents were captured, marked by toe clipping, and released (Table 1). Trapping data were analyzed using stepwise discriminant analysis (Dixon, 1970). For analysis, each trap station was given an X, Y co-ordinate. X axis trap rows ran parallel to the dune-valley boundary; Y axis trap rows were at right angles to the boundary. Y ordinates one through seven were located on valley floor, eight through fourteen on dunes. The X, Y co-ordinates defined the location of each rodent capture and were the basis upon which distributions were separated. During this study Dipodomys deserti was almost entirely restricted to dune substrate during both time periods (Fig. 1). Previous work has indicated that this is optimum habitat for the desert kangaroo rat (Grinnell, 1922; Durrant, 1943; Butterworth, 1960; Eisenberg, 1963). Most workers consider D. deserti to be one of the most specialized kangaroo rats (Grinnell, 1922; Wood, 1935; Lidicker, 1960), and this specialization was reflected in the strong substrate preference which did not change with habitat quality. “Before” and “after” distributions of D. deserti were significantly different from the other two species distributions; however, separation increased in the “after” period (Table 2). During the “before” period Dipodomys merriami was captured in both habitats, but its initial distribution was significantly different when compared to the “after” period (Fig. 1). TaBLE 2.—Stepwise discriminant analysis F-matrix comparing three species distributions in two time periods. * significant F-value at the 0.05 level. D. deserti D. merriami ee re ee SS BEFORE 15 AUGUST RAIN D. merriami 3.5006* P. longimembris 3.0916* 0.1001 AFTER 15 AUGUST RAIN D. merriami 32952" P. longimembris 14.4996* 2.7976 359 August 1974 GENERAL NOTES 661 Tale 13 12 le. Dune O1833 9 8 . 5 0.4490 6 So 5 12 77g 4 Valley 3 fe V D. desert 2 [] D merriami 1 Gar longimembris Before After Fic. 1.—Results from an analysis of variance of changes in rodent distribution from “before” to “after” time periods. One through 14 on the Y axis represent trap rows. Symbols indicate mean Y axis distribution. * significant F-value at the 0.05 level. The difference in between-period distribution of D. merriami was caused by its withdrawal from the dunes during the “after” period. Due to the extreme conditions during the “before” period, I suggest that withdrawal from the dunes during the period of plant growth and seed production was related to the increasing availability of food resources in areas not occupied by the dominant D. deserti. Lidicker (1960) found that although sandy soils are preferred, D. merriami will tolerate a wide range of soil types with the presence of open areas being the most important factor affecting its distribution. Open areas were present in both habitat areas of the trap grid and are, therefore, not considered to be important in determining the local distribution of Merriam’s kangaroo rat. During both periods Perognathus longimembris was found in both habitats almost equally (Fig. 1). Interaction with kangaroo rats does not appear to be a major factor in determining its distribution. Separation may be related to feeding behavior as was noted for Dipodomys heermanni and Perognathus parvus which took different seeds where they occur sympatrically (Smith, 1942). Brown and Lieberman (1973) have shown that D. deserti, D. merriami, and P. longimembris harvested seeds of different sizes; however, there was considerable overlap between the seeds harvested by D. merriami and P. longimembris. They also showed that the kangaroo rats forage primarily on the open ground away from vegetative cover, whereas P. longimembris concentrated its foraging under the cover of shrubs. For a detailed discussion of rodent species diversity on sand dunes and resource utilization by the species see Brown (1973) and Brown and Lieberman (1973). The important point shown by this study is that investigators should be careful to note habitat conditions when making short-term samples of rodents for purposes of 360 662 JOURNAL OF MAMMALOGY Vol. 55, No. 3 determining distribution or spatial relationships between species as these relationships may change with habitat quality. I thank Dr. Richard MacMillen and my committee members for assistance with this research. This paper is part of a thesis submitted in partial fulfillment of the requirements for the degree of Master of Science at California State Polytechnic University. LITERATURE CITED Brown, J. H. 1973. Species diversity of seed-eating desert rodents in sand dune habitats. Ecology, 54:775-787. Brown, J. H., ano G. A. LizpermMan. 1973. Resource utilization and coexistence of seed-eating desert rodents in sand dune habitats. Ecology, 54:788-797. BurTreRworTH, B. B. 1960. A comparative study of sexual behavior and reproduction in the kangaroo rats Dipodomys deserti (Stephens) and Dipodomys merriami (Mearns). Unpublished PhD dissertation, Univ. Southern California, 169 pp. Dixon, W. J. 1970. BMD Biomedical Computer Programs. University of Calif. Press, Berkeley, 600 pp. Durrant, S. D. 1943. Dipodomys deserti in Utah. J. Mamm., 24:404. EISENBERG, J. F. 1963. The behavior of heteromyid rodents. Univ. California Publ. Zool., 69:1—100. GRINNELL, J. 1922. A geographical study of the kangaroo rats of California. Univ. California Publ. Zool., 24:1-124. LipickerR, W. Z. 1960. An analysis of intraspecific variation in the kangaroo rat Dipodomys merriami. Univ. California Publ. Zool., 67: 125-218. Smitu, C. F. 1942. The fall food of brushfield pocket mice. J. Mamm., 23:337-339. Woop, A. E. 1935. Evolution and relationships of the heteromyid rodents with new forms from the Tertiary of western North America. Ann. Carnegie Mus., 24:73-262. Justin Concpon, Box 6, Department of Zoology, Arizona State University, Tempe, 85281. Submitted 16 October 1973. Accepted 29 January 1974. 361 378 JOURNAL OF WILDLIFE MANAGEMENT, VOL. 20, No. 4, Ocroper 1956 CHANGES IN NORWAY RAT POPULATIONS INDUCED BY INTRODUCTION OF RATS David E. Davis and John J. Christian Division of Vertebrate Ecology, Johns Hopkins School of Hygiene and Public Health, Baltimore 5; Naval Medical Research Institute, Bethesda, Maryland The introduction of aliens into an existing population of mammals may be followed by unexpected effects that relate to social structure and population composition. These effects were studied by introducing alien rats into stationary and increasing popula- tions of rats in city blocks. This work is part of a continuing study of the mechanisms of change in vertebrate populations using Nor- way rats (Rattus norvegicus) in residential areas in Baltimore as experimental animals (Davis, 1953). These rats inhabit back yards, basements, and garages and feed on garbage. The human sanitary conditions in general are poor and remain unchanged for months at a time, so that the food supply of the rats has only slight seasonal variations. Other environmental conditions are similarly sub- ject to little change for many months at a time. The constancy of these factors permits experiments on populations in a relatively stable environment. Finally, the population of rats in each block is essentially discrete and isolated, as rats rarely travel from one block to another (see Davis, 1953, for refer- ences ). METHODS AND PROCEDURES The procedures followed to study the ef- fects of introducing strange rats into a popu- lation consisted of taking some rats from a stationary or increasing population in one block and introducing them into a compara- ble population in another block and observ- ing the resulting changes in the second pop- ulation. The status (stationary or increasing) of the population was determined by esti- mates at bimonthly intervals for more than a year. Blocks that appeared to be either stationary or increasing were selected in October and monthly estimates made. From this group 4 stationary and 4 increasing pop- ulations were chosen. To get a base line for adrenal weights, six rats of one sex, weighing over 200 grams each, were removed from each block during the first experimental week (week 1). Alien rats were then intro- duced into each block during the third week, and at the same time native rats were re- moved from the increasing populations. The details of these removals and introductions are contained in tables 2 and 3. Estimates were made during the sixth and eighth 362 CHANGES IN Rat PopuLtations—Davis and Christian weeks, each followed by the removal of a small sample of rats for adrenal weights. The adrenal weights were expressed for each sample as the mean per cent of standard reference values (Christian and Davis, 1955). The rats to be introduced into a population were individually marked by toe-clipping prior to introduction, whereas the native rats were not marked. The details of the history of each population were complicated by the impossibility of introducing exactly the same number of rats into each block on exactly the same days, and the numerical popula- tion size also differed in each block. A discussion of the likelihood of error is desirable when it is claimed that two popu- lations differ in number, since the detection of changes is fundamental to the conclusions derived from these introductions. Some as- pects of the census method were discussed by Brown, et al. (1955). However, the basic problem is that, even with trapping, the true number of rats in a block is not known. Nevertheless, a check on the validity of esti- mation can be made by comparing estimates before and after a trapping program. Sup- pose that an estimate of N, rats is first ob- tained, subsequently T rats are removed and a second estimate of N, rats is made. Obviously N, should equal T + N.. A figure for percentage of error can be given as Niece t au No): 7 ae Ne), For example, if the estimate 1 for a block is 151 rats and then 81 are re- moved by trapping and an estimate of 63 15i— (Sh 63) 151 cent. Other procedures could be used such as ae NG) af Ny) or piss shatiNe i = The first procedure is preferred because it bases the calculations on N,, which is the estimate that was used to determine the status of the block. A total of 50 populations was avail- able to determine the extent of error. Each had been trapped during the past 6 years, and an estimate had been made before trap- ping and another within a month after ces- sation of trapping. Naturally, some changes can occur during the intervening month, but for practical reasons it is usually not possible to make an estimate promptly after the ces- sation of trapping. These blocks contained 3,707 rats by the estimates (N,) and 1,502 were trapped. The number of rats per block is made, then = 46 per 379 TABLE 1. — DisTRIBUTION OF DIFFERENCES AMONG EsTIMATES Blocks Per cent Error® Positive Negative Total 0-9 13 6 19 10-19 6 iLil 17 20-29 4 4 8 30-39 2, 3 5) 40-49 1 0 1 Totals 26 24 50 * Ni — (T + Ne) Ni varied from 15 to 182. The distribution of errors is given in Table 1. The percentage of error was independent of the number of rats in the population. From these differ- ences the standard error of the difference can be calculated to be 10.7 per cent. This value can be used as an indication of the errors to be expected in estimates of popula- tion changes in blocks. For example, from Table 2 it is seen that the estimate (block 150128) before introduction was 116 and after was 89. The percentage difference is 23.3 which when divided by 10.7 gives a ratio of 2.2. This difference appears to be statistically significant. RESULTS AND DISCUSSION The histories of the populations are given by blocks in tables 2 and 3 and figures 1, 2, and 3. The terms “replacement” and “sup- plement” require clarification for this dis- cussion. We mean by replacement that ap- proximately the same number of rats was introduced as was removed. Supplement means that many more alien rats were intro- duced than were removed. A quantitative percentage might have been used to dis- tinguish these two terms, but it would have been rather meaningless because (1) the size of the individual rats varies consider- ably, and (2) immediate mortality is prob- ably high. Therefore, we really do not know the actual number of rats that produced the results. Another factor is that births and deaths are normally high in any population of rats. The average monthly death rate is about 20 per cent for stationary rat popula- tions; therefore, their birth rate is also about 20 per cent. Comparable mortality and birth rates for increasing populations are prob- 363 380 JOURNAL OF WILDLIFE MANAGEMENT, VOL. 20, No. 4, OCTOBER 1956 TABLE 2.— RESULTS OF INTRODUCTION OF RATs INTO STATIONARY POPULATIONS Block number........- 140338 140344 140118 150128 LEXOV WEEK AS ie) sconces aratves i=) 2s Dec. 16 Dec. 16 Feb. 9 Feb. 9 Week Rats Ww R Ww R w R Population —20 62 —20 30 —19 105 —18 122 Population —13 42 —13 32 —ll 98 —10 118 Population — 5 40 — 5 38 — 6 87 — 6 120 Population 0 49 0 35 0 100 0 116 Rats removed 1 6M 1 6F if 6F 1 6M Rats introduced 3 10M 3 8F 2-6 23F 2-6 27M Rats removed = — — — — — — - Population 6 45 6 44 6 76 7 89 Rats removed 6 6M 6 6F 6 6F 7 6M Population 8 56 8 23 ll 63 10 86 Rats removed 8 22 8 12 1l 27 10 36 Week Index1 WwW I W I WwW I 1 83.0 1 91.8 1 93.4 it 79.2 Adrenal size 6 84.1 6 85.3 6 90.4 7 71.4 8 88.0 8 102.4 11 68.4 10 73.6 1 Mean of the individual per cent of appropriate reference value for the sex and size of the rat. ably about 15 per cent and 25 per cent per STATIONARY month respectively. It is unwise, under these circumstances, to attempt a precise measure- ISO aber ment of numerical differences in the num- \ bers of rats used. ‘ The population estimates (Table 2) in 125 150128 & all \ the two replacement blocks 6 weeks after ee” © \+23 the introduction of rats showed (Fig. 1) that e \ block 140338 was not significantly different 140118 ¢ van from the previous estimate, while block 100 = iB ate: : : \ 140344 had apparently increased (P is about a Vat 04). While the apparent difference in re- 2 Ne ie ie sults in these 2 blocks might be due to sex as (the females less disturbing) or to numbers 4 7. x (fewer introduced into 140344), no inter- @? ae pretation will be attempted for the reasons 40336 6 tH cited above. The two supplemented blocks z -|6 x declined significantly (P is about .04 for & 50 a ihc One, each) (Fig. 1). ne ae We recognize that the replacement pair of 4 eh populations was done in December 1953, , ee i \ and the supplemented pair in February 1954, 25 140344 9 E, : HN and that differences might be due to some 3 seasonal aspect. However, the only known seasonal change, an increase in breeding from December to February, would produce the opposite result. Population growth ceased in all four in- creasing populations following the replace- ment of native with alien rats (figs. 2, 3,). In no block was the difference statistically significant. It apparently made no differ- ence whether the sex of the introduced rats fe) -30 -20 -l0 0 10 WEEKS Fic. 1. The changes in four stationary populations for 20 weeks before introduction of rats (at 0 time) and about 10 weeks after. The number added is indicated by a plus sign, the number removed by a minus sign. 364 CHANGES IN Rat PopuLations—Davis and Christian 381 TABLE 3.— RESULTS OF INTRODUCTION OF RATS INTO INCREASING POPULATIONS Block number......... 140111 140134 140201 140222 Zero week is.......... Dec. 16 Dec. 16 Feb. 9 Feb. 9 Week Rats W R W R W R Population —20 110 —20 80 —25 86 —20 Dili Population —13 118 —13 88 —16 100 —14 62 Population —5 133 —4 115 — 8 105 —5 95 Population 0 150 0 140 0) 135 0 90 Rats removed i 6F 1 6F 1 6M i 6M Rats introduced 3 22F So 28 3 18M S 20M Rats removed 3 28F 3. 22F 3 20M 3 18M Population 6 167 6 130 6 130 6 85 Rats removed 7 6F 7 6F 7 6M 7 6M Population 10 152 10 130 10 130 10 70 Rats removed 10 48 10 vis 10 57 10 24 Week Index1l W i Ww I W I 1 92.1 1 91.5 1 104.4 1 93.8 Adrenal size “i 93.8 7 102.8 1 85.3 if 99.1 10 101.5 10 90.4 10 91.1 10 84.6 1 Mean of the individual per cent of appropriate reference value for the sex and size of the rat. was male or female. The population from 150 block 140222 (Fig. 2) may have become Pe stationary just prior to the introduction of —6|20 aliens, but the high rate of reproduction (4/6 i mature females were pregnant) suggests that 125 the population was increasing. The popula- tion in block 140111 increased numerically after the introduction, but the difference be- 140201 . tween the two estimates is within the error 100 e =6|420 of estimate and does not indicate a change a i 1-18 in population. It appears that introducinga §& ° Naa Fe number of alien rats may halt the growth of & * increasing populations. 2 ue ~ The reader may have noticed that the total 9% a number of rats removed from the four in- © 140222 creasing blocks was about 5 per cent greater & ———* than the number introduced, so that the rats in these populations were not replaced in the strict arithmetic sense of the word. However, considering the previously mentioned birth and mortality factors, it is not desirable to be more precise. All aspects considered, it is likely that the four increasing populations were somewhat reduced following replace- ment procedures. The four blocks (taken together) increased by 173 rats in the 20 weeks preceding replacement, so that they might have been expected to have had 600 rats 10 weeks after replacement instead of the observed 482, although the rate of in- crease would decline as the population in- creased. On several occasions episodes have been noted that appear to be explainable on the -20 -10 10 WEEKS Fic. 2. The changes in two increasing blocks before and after the introduction of males (symbols as in Fig. 1.) basis of introduction or actual immigration. In January 1946, about 60 rats were released in a block in one night as part of an experi- 365 382 175 +22 pe 7% ce -6 N 150 “ > Ws +28 Va —22 @ are 125 0 , a. 140ll! e@ ee x ® 100 140134 a ° x < ae =. 75 a (o) a = q = 50 25 FEMALES 050 -20 -10 0 10 WEEKS Fic. 3. The changes in two increasing blocks before and after the introduction of females (symbols as in Fig. 1.) ment on “homing” ability in rats. The block originally contained about 100 rats but with- in 3 weeks there were so few rats left in the block that the project was stopped. Calhoun (1948) noticed the same result when he in- troduced rats into blocks. These episodes, as well as miscellaneous observations, stim- ulated a test in 1947 of the idea that the in- troduction of rats into a population would result in its decline. Accordingly, rats were introduced over a period of 4 months into two populations that had just reached a level judged to be stationary (Davis, 1949). The introduction of 90 rats in one block and 101 in the other was accompanied by declines of about 25 per cent and of 40 per cent respec- tively. The populations increased after the introductions ended. The present experiments suggest that the introduction of large numbers of rats into a population disrupts the population mech- JOURNAL OF WILDLIFE MANAGEMENT, VOL. 20, No. 4, OcroBER 1956 anisms in some way that causes the popula- tions either to decline in numbers or stop growing. The decrease is due in part to a decline in reproduction. Data are not available for the period immediately after introduction, as it is not feasible to follow the population changes and simultaneously to collect a number of rats for reproductive data. However, the large sample of rats collected from the blocks 8 to 11 weeks after introduction had a high reproductive rate (Table 4) and a low lacta- tion rate. One would conclude from these data that the number of pregnancies was low immediately after the introduction. Only about 25 per cent of the females were lacta- ting at 10 weeks, whereas normally about 40 per cent of the females of these rats are lactating (Davis, 1953). The high preva- lence of pregnancy presumably resulted from their more or less simultaneous re- covery from the effects of introduction. The decreases in rat populations obviously may have been due largely to mortality and move- ment, but data on this aspect are impossible to obtain under these conditions. TABLE 4. — REPRODUCTIVE RECORDS OF LOCAL RATS CaptTuRED 8-11 WEEKS AFTER ARTIFICIAL IMMI- GRATION OF RATs INTO BLOCKS Number Mean Population Mature Per cent Number Per cent status Females Pregnant Embryos Lactating Increasing 85 33.0 10.38 20.0 Stationary 66 31.8 9.63 28.8 Previous experiments have shown that the weight of the adrenal glands in rats responds to changes in population. An increase in adrenal weight parallels increases in popu- lation; the artificial reduction of a popula- tion also results in a decrease in adrenal weight (Christian, 1954; Christian and Davis, 1955). The adrenal responses of the two sexes are parallel (ibid.). Experiments have indicated that changes in adrenal weight in response to changes in population result primarily from changes in cortical mass (Christian, 1955a, 1955b, 1956). To examine these problems, the adrenals of the rats from each block were removed and weighed. The observed adrenal weight for each rat was compared with a standard reference weight for the appropriate sex and size (length of head and body ) of rat (Christian and Davis, 366 CHANGES IN Rat PopuLations—Davis and Christian 1955), and expressed as a per cent of the reference value. These percentages for the rats from each sample were averaged an the means are recorded at the bottom of tables 2 and 3. We have used the mean value of a given sample as the unit of measurement for comparing adrenal weight with popula- tion size (Christian, 1954; Christian and Davis, 1955). The results indicate that, in the replace- ment stationary blocks (140338 and 140344), there was a small increase in adrenal weight after 8 weeks, while the populations appar- ently remained practically unchanged (ta- bles 2 and 3, Fig. 1). A mean decline in population size, par- alleled by a decrease in adrenal weight in at least one of the two blocks, followed the addition of a large number of alien rats to stationary populations (blocks 140118 and 150128). The adrenal weights probably re- flect largely the final results of population manipulation rather than the immediate ef- fects, as the adrenal samples were obtained several weeks after the introductions or esti- mates. Therefore, the changes in adrenal weight probably reflect overall population changes rather than any immediate social strife resulting from the introductions. An experiment to collect samples a few days after the introductions is in progress and may show an increase in adrenal weight. The adrenal glands of rats from the in- creasing blocks showed no consistent change, although population growth terminated (Ta- ble 3, figures 2 and 3). The replacement of rats in increasing populations had little ef- fect on the adrenal weights of rats examined 10 weeks later. The results reported here may be applica- ble to certain stocking programs. A routine part of many game-management programs has been the introduction of a number of animals into an area with the expressed hope of increasing the population either directly or eventually by reproduction. Indeed, such stocking has often been considered a pana- cea for all hunting problems. The present results, using rats as experimental animals, show that the disruption of a population following an introduction may actually pro- duce a decline under certain conditions. Evi- dently the introduction of a number of ani- mals may have disastrous results when a population is above the halfway point on a growth curve. 383 SUMMARY Wild Norway rats (Rattus norvegicus ) were introduced from one city block to an- other to simulate immigration. The pop- ulation changes were determined by fre- quent estimates for about 20 weeks before introduction and 8 to 11 weeks thereafter. From two blocks with stationary rat popula- tions, some rats were removed and then replaced by aliens. The populations re- mained stationary. In two blocks about four times as many rats were introduced as were removed. The populations declined about 25 per cent. In four blocks with increasing populations about one-fourth of each pop- ulation was removed and replaced by alien rats from other blocks. The increase halted. The reproductive rate 8 to 11 weeks after the introduction was normal for an increas- ing population, but the lactation rate was low, indicating that the decline in popula- tion growth was due in part to a decreased reproductive rate, and that the population was back to normal pregnancy rate in two months. The adrenal weights were also es- sentially normal for the population level two months after introduction. REFERENCES Brown, R. Z., W. SALtow, Davip E. Davis, AND W. G. Cocuran. 1955. The rat population of Baltimore 1952. Amer. J. Hyg., 61(1):89-102. CaLHoun, J. B. 1948. Mortality and movement of brown rats (Rattus norvegicus) in artificially super-saturated populations. J. Wildl. Mgmt., 12(2):167-172. CurisTIAN, J. J. 1954. The relation of adrenal size to population numbers of house mice. Sc. D. dissertation, Johns Hopkins Univ., Baltimore. . 1955a. Effect of population size on the adre- nal glands and reproduction organs of male mice in populations of fixed size. Amer. J. Physiol., 182(2) :292-300. 1955b. Effect of population size on the weights of the reproductive organs of white mice. Amer. J. Physiol., 181(3) :477-480. ———. 1956. Adrenal and reproductive responses to population size in mice from freely growing populations. Ecology, 37(2):258-273. —--— AND D. E. Davis, 1955. Reduction of adrenal weight in rodents by reducing population size. Trans. N. Amer. Wildl. Conf., 20:177-189. Davis, D. E. 1949. The role of intraspecific compe- tition in game management. Trans. N. Amer. Wildl. Conf., 14:225-231. . 1953. The characteristics of rat populations. Quart. Rev. Biol., 28( 4) :373-401. Received for publication October 24, 1955. 367 A TRAFFIC SURVEY OF MICROTUS-REITHRODONTOMYS RUNWAYS By O.iver P. PEARSON Patient observation of the comings and goings of individual birds has long been one of the most rewarding activities of ornithologists. The development in recent years of inexpensive electronic flash photographic equipment has made it possible and practical for mammalogists to make similar studies on this aspect of the natural history of secretive small mammals. The report that follows is based on photographic recordings of the vertebrate traffic in mouse runways over a period of 19 months. Species, direction of travel, time, temperature and relative humidity were recorded for each passage. In addi- tion, many animals in the area were live-trapped and marked to make it possible to recognize individuals using the runways. THE APPARATUS Two recorders were used. Each consisted of an instrument shelter and a camera shelter. Each instrument shelter was a glass-fronted, white box con- taining an electric clock with a sweep second hand, a ruler for measuring the size of photographed individuals, a dial thermometer and a Serdex membrane hygrometer. The ends of the box were louvered to provide circulation of air as in a standard weather station. This box was placed along one side of the runway, across from the camera shelter, so that the instruments were visible in each photograph (Plate I). The camera shelter was a glass-fronted, weather- proof box containing a 16-mm. motion picture camera synchronized to an electronic flash unit. In one of the recorders the camera was actuated by a counterweighted treadle placed in the mouse runway immediately in front of the instrument shelter (Plate I, bottom). An animal passing along the runway depressed the treadle, thereby closing an electrical circuit through a mercury-dip switch. This activated a solenoid that pulled a shutter-release pin so arranged that the camera made a single exposure. The electronic flash fired while the shutter was open. This synchronization was easily ac- complished by having the film-advance claw close the flash contact. The camera would repeat exposures as rapidly as the treadle could be depressed, but at night about three seconds were required for the flash unit to recharge sufficiently to give adequate light for the next exposure. 169 368 170 JOURNAL OF MAMMALOGY Vol. 40, No. 2 The other recorder was actuated by a photoelectric cell instead of by a treadle. A beam of deep red light shone from the camera shelter across the runway and was reflected back from a small mirror in the instrument shelter to a photoelectric unit in the camera shelter. When an animal interrupted the light beam, the photoelectric unit activated a solenoid that caused the camera to make a single exposure, as in the other recorder. To avoid the possibility of frightening the animals it would be desirable to use infra-red-sensitive film and infra-red light, but standard electronic flash tubes emit so little energy in the infra-red that this is not practical. Instead, I used 18 layers of red cellophane over the flash tube and reflector to give a deep red flash of light. Wild mice, like many laboratory rodents, are probably insensitive to deep red light. I found no evidence that the flash, which lasts for only 1/1000th of a second, frightened the mice. A muffled clunk made by the mechanism also seemed not to alarm the mice unduly. When the camera diaphragm was set to give the proper exposure at night, daytime pictures were overexposed, since the shutter speed was considerably slower than 1/30th of a second. To reduce the daytime exposure, a red filter was put on the camera lens. The filter did not affect night exposures because red light from the flash passed the red filter with little loss. In addition, on one of the cameras the opening in the rotary shutter was reduced to give a shorter exposure. Both recorders function on 110-volt alternating current. The treadle-actuated one could be adapted to operate from batteries. The units continue to record until the motion picture camera runs down or runs out of film. One winding serves for several hundred pictures. The film record can be studied directly by projecting the film strip without making prints. The camera shelter and instrument shelter had overhanging eaves to prevent condensation of frost and dew on the windows. A small blackened light bulb was also kept burning in the camera shelter to raise the temperature enough to retard fogging on the glass. Animals were encouraged to stay in their usual runway by a picket fence made of twigs or slender wires. No bait was used. A few individual animals could be recognized in the pictures by scars or molt patterns, but most had to be live-trapped and marked. Using eartags and fur-clipping I was able to mark distinctively (Plate I, bottom) all of the mice captured at any one station. The clipping remained visible for days or months depending upon the time of the next molt. The apparatus produces photographic records such as those shown in the lower pictures in Plate I. These can be transposed into some form as Fig. 2. THE STUDY AREA The study centered around a grassy-weedy patch surrounding a brush pile in Orinda, Contra Costa County, California (Plate I). The runways wound through a 20 x 20-foot patch of tall weeds (Artemisia vulgaris, Hemizonia sp. and Rumex crispus) and under the brush pile. The weeds were surrounded 369 May, 1959 PEARSON—TRAFFIC SURVEY 171 by and somewhat intermixed with annual grasses. Oaks and other trees, as well as a house and planting, were 50 feet away. Summer climate in this region is warm and sunny with official mean daily maximum temperatures rising above 80°F. in late summer. Official temper- atures occasionally reach 100°, and temperatures in the small instrument shelters used in this study sometimes exceeded this. Nights in summer are usually clear and with the mean daily minimum temperature below 52° in each month. About 27 inches of rain fall in the winter and there is frost on most clear nights. The mean daily maximum temperature in January, the coldest month, is 54°, and the mean daily minimum 31°. PROCEDURE I placed the first recorder in operation on January 29, 1956, and the second on October 19, 1956. Except for occasional periods of malfunction and a few periods when I was away they continued to record until the end of the study on September 10, 1957. Approximately 778 recorder-days or 111 recorder- weeks of information were thus obtained. The monthly distribution of records was as follows: January, 54 days; February, 70; March, 90; April, 80; May, 84; June, 67; July, 52; August, 88; September, 48; October, 33; November, 52; and December, 60. The recorders were placed at what appeared to be frequently used Microtus runways, usually situated on opposite sides of the weedy patch 20 to 30 feet apart. For one period of four months one of the recorders was placed at a similar weedy patch 70 yards away. Early in the study it was discovered that a neighbor’s Siamese cat sometimes crouched on the camera shelter waiting for mice to pass along the exposed runway in front of the instrument shelter. Consequently, a 214-foot fence of 2-inch-mesh wire netting was set up enclosing most of the weedy patch. This prevented further predation by cats at the center of the study area, although cats continued to hunt outside of the fence a few yards away from the recorders. The only other tampering with predation was the removal of two garter snakes on April 11, 1957. RESULTS Traffic in individual runways.—The recorders were operated at eighteen different stations. At seven of these apparently busy runways a traffic volume higher than a few passages per day never developed, and so the recorders were moved within two weeks. Perhaps the mice originally using these runways had abandoned them or had been killed shortly before a recorder was moved to their runway, or perhaps the disturbance of placing a recorder caused the mice to divert their activities to other runways. At the other eleven stations a satisfactory volume of traffic was maintained for three to more than twenty weeks. A station was abandoned and the recorder moved when the traffic had decreased to a few passages per day. Subsequently, I found that even this little activity does not indicate that the mice are going to abandon the runway, 370 172 JOURNAL OF MAMMALOGY Vol. 40, No. 2 for on several occasions traffic in a runway dropped this low and then climbed again to high levels. At one recorder the total number of passages in consecutive weeks was 183, 84, 26, 75 and 203. The runway represented in Fig. 1 was one of those used most consistently, but even it shows marked daily and weekly fluctuations. It is probable that after a few weeks of disuse during the season when grass and weeds are growing rapidly, a runway would not be reopened, but during the rest of the year an abandoned runway remains more or less passable and probably more attractive to mice than the surrounding terrain. Figure 1 summarizes the traffic in one of the busiest runways. On the first night there were an unusual number of records of harvest mice whose curiosity may have been aroused by the apparatus. Obviously they were not frightened away. After a short time traffic increased to a high level and remained high until the middle of November, when passages by Microtus decreased sharply. During the week before the decrease, seven marked individuals provided most of the Microtus traffic. One of these individuals, an infrequent passerby, dis- appeared at the time of the decrease, but the other six remained nearby for at least another week and continued to pass occasionally. Those Microtus that disappeared later were replaced by others so that even the infrequent passages in late November and early December were being provided by seven marked individuals. The decrease of Microtus traffic was caused, therefore, not by deaths but by a change in runway preference. Several of these same individuals were using another runway 20 feet away in mid-January, February and March. Three to six marked Reithrodontomys, depending upon the date, were pro- viding most of the harvest-mouse traffic in the runway represented in Fig. 1. The average number of passages per day of animals of all kinds was eighteen. In the ten other most successful runways, the average number of passages per day ranged from two to nineteen. Figure 2 gives a detailed accounting of the traffic at a single recording station for six days. One can judge from this figure the kind of information (excluding f] © OTHER fA « MEADOW MICE AA «HARVEST MICE MAA AMIN SS RAVAN AAA AAAAAAL WH RMAAQAAHARANN RAH RsaI SAA AAAAAG|M|-I_AyAFTA MAMA NUMBER OF PASSAGES RRR RQ QA RARMAAAAAA ON SSAA RVAAAAVAAAMAAAAANI DA BQAQ QOQiVa73w x SWAMAAAA AAAI AN RRAEEANNN 16 30 15 31 1S 30 15 31 OCTOBER NOVEMBER DECEMBER Fic. 1.—Traffic volume along one runway for 16 weeks. Meaning of symbols under the base line: T= live-trapping carried out for part of this day; O= full moon; E= total eclipse of the moon; R= rain. Columns surmounted by a vertical line represent days for which the recording was incomplete; the heights of the various segments of these columns should be considered minimum values. 371 May, 1959 PEARSON—TRAFFIC SURVEY 173 temperatures and humidities) obtained with the recorders and can at the same time catch a revealing glimpse of an aspect of the biology of small mammals that has heretofore been revealed inadequately by trapping and other techniques. lt may be seen that the mouse traffic was provided by one female and two male harvest mice and by three male, three female, and one or more unidentified meadow mice; together they gave between 15 and 24 passages each day. No individual passed more than eight times in one day. One harvest mouse (R2) seemed to spend the day to the left and to make a single excursion PLATE. I Top: Camera shelter (foreground) and instrument shelter in position at a mouse runway on the study area. Borrom: The kind of records obtained with the recorder; left—a meadow mouse marked by clipping two strips of fur on the hips; right—a marked harvest mouse crossing the treadle. 372 174 JOURNAL OF MAMMALOGY Vol. 40, No. 2 to the right each night. Harvest mice first appeared in the evening between 6:37 and 7:22 and none passed after 6:26 in the morning. Five or six Microtus passed within a few hours (February 24), and there was nightly near-coinci- dence of Reithrodontomys and Microtus. Traffic in all runways combined.—During the 111 recorder-weeks, the follow- ing passages of animals were photographed: Meadow mouse, Microtus californicus 6,077 Harvest mouse, Reithrodontomys megalotis 1,753 Bird (see following account ) 382 Brush rabbit, Sylvilagus bachmani 94 Shrew, Sorex ornatus 56 Peromyscus (see following account ) 39 Fence lizard, Sceloporus occidentalis 33 Garter snake, Thamnophis sp. 17 Salamander (see following account ) ume Alligator lizard, Gerrhonotus sp. 10 House cat, Felis domesticus 6 Newt, Taricha sp. 5 Pocket gopher, Thomomys bottae 3 Gopher snake, Pituophis catenifer 3 Mole cricket, Stenopelmatus sp. 2 Ground squirrel, Citellus beecheyi I Weasel, Mustela frenata 1 King snake, Lampropeltis getulus ] Racer, Coluber constrictor 1 TOTAL 8,495 On the basis of trapping results in this and in similar habitat nearby, large numbers of meadow mice and harvest mice were expected. The recording of at least 26 other species in the runways came as a pleasant surprise. Whereas all of these species would be expected to record their presence eventually, some of them are rarely seen or trapped near this location. After living five years on the study area, after doing considerable field work nearby, and after checking the recorders twice each day during the study, I have not yet seen a weasel or a ground squirrel within at least a mile of the study area. Weasels could easily escape detection, but large, diurnal ground squirrels must be very rare. The single individual recorded on August 31 may have been a young squirrel emigrating from some distant colony. Noteworthy absences were those of wood rats (Neotoma fuscipes), moles (Scapanus latimanus ), and probably California mice (Peromyscus californicus), all of which were common within 100 feet of the recorders. An opossum (Didelphis marsupialis ) was seen a few feet from one of the recorders but did not appear on the films. No house mice (Mus musculus) were detected in the photographs, although 373 May, 1959 PEARSON—TRAFFIC SURVEY 175 it is possible that some passages of Mus were listed as of Reithrodontomys. House mice were caught occasionally in houses nearby and in a field near a poultry house 200 yards away, but none was caught during frequent live- trapping near the recorders. The total of 8,495 passages of animals gives an average of 11 passages per day in each runway. A patient, non-selective predator waiting for a single catch at runways such as these could expect, theoretically, a reward each 2.2 hours. The mean weight of animal per passage was about 31 grams, which would yield approximately 40 calories of food. This much each 2.2 hours would be more than enough to support an active mammal the size of a fox. Meadow mouse.—The 6,077 Microtus passages were distributed throughout the day and night as shown in Fig. 3 (above). The hours of above-ground activity, however, were quite different in winter than in summer, so Fig. 3 is only a year-around average somewhat biased by the fact that more Microtus were recorded in the spring than in the other seasons. A more detailed analysis of the Microtus data will be given in a later report. By marking as many of the mice as possible, it was found that usually four or more individual Microtus were using each runway but rarely more than ten. On some occasions more than 60 Microtus passages were recorded at a single point in 24 hours. Harvest mouse.—Harvest mice were almost entirely nocturnal (Fig. 3, center). They not only used the Microtus runways, but their passages were frequently intermixed with those of Microtus (Fig. 2). On fourteen occasions the two species passed within 60 seconds of each other, and on one occasion 6 7 8 9 10 tt NOON 1 2 3 4 5 6 7 8 9 10 th NIGHT | 2 3 4 5 FEB. 41 tt 24-25 R MB MoM MoM M MM MM R M M MM MM MM RMRR 5 6 6 5 5 76 §8 3 5 9 7567 85 2533 9 co) 66 66 gg 69 6 3G to 9d SQ QA Qddd 8B M B OM MM M R RRM R M M M M M 5 345 3 5 5 7258 § 6 ¢ ¢ ¢8 é § ada ¢ & ¢ 9488 3 ¢ FEB. 28— R ee oe cr ae ee ee 9d Y Qdod 5 2 999 g 9 dQ 95g go 6 fi 8 oe 10 11 NOON | 2 3 4 5 6 7 8 9 ite) (1 NIGHT | 2 3 4 5 6 Fic. 2.—A sample record of the total traffic in a single runway over a period of six days. Marks above the base lines indicate passages from right to left, and marks below the base line passages from left to right. R represents Reithrodontomys; M, Microtus; B, bird (includes brown towhee, wren-tit, and song sparrow); and RAB, brush rabbit. Most of the mice are further identified by number and sex. 374 176 JOURNAL OF MAMMALOGY Vol. 40, No. 2 a 4-month-old male Microtus and a 5-month-old male Reithrodontomys ap- peared in the same photograph. The history of one runway indicates that traffic by Reithrodontomys alone does not keep a Microtus runway open. One or more Microtus passed almost daily along this runway during February. At the end of the month the Microtus disappeared and two Reithrodontomys became active in the same runway. Despite an average of 3.3 passages per day by Reithrodontomys throughout March and up to mid-April, grass and weed seedlings grew up MEADOW MICE = £10 ALL MONTHS 5 N= 6077 ra 5 me W cc ice 678se9 0 l2t12345 6789 100 1212345 6 NOON NIGHT HARVEST MIGE J ALL MONTHS N = 1753 Oo za uJ => (e] uJ a Ww 6, 7 6: 9>. 1OTi2: Wi ce 23 94. 5126 7 6B SIO NLA A 2S 4 5 6 NOON NIGHT BRUSH RABBIT N= 94 FREQUENGY (%) 657859. iO Nei2 Wh) 2 3-4. 5 6 7. 8-8 10 Ne 2 2) 2") 4 SoG NOON NIGHT Fic. 3.—Distribution by hours of 6,077 passages of meadow mice (above); 1,753 passages of harvest mice (center); and 94 passages of brush rabbits (below). 375 May, 1959 PEARSON—TRAFFIC SURVEY Mare in the runway and it began to look unused. By the end of April almost all traffic had ceased. The Reithrodontomys data will be analyzed in a later report. Birds.—Of the 382 bird records, at least 255 were of sparrows (at least 122 song sparrow; the remainder mostly fox sparrow, white-crowned sparrow and golden-crowned sparrow ). Other birds recognized were wren-tit, wren, brown towhee and thrush. On several occasions birds, especially song sparrows, battled their reflections in the window of the instrument shelter. This caused long series of exposures. Each series was counted as a single passage. If the bird stopped for a minute or more and then returned to the battle, this was counted as another passage. All bird records were during daylight hours. On three occasions a sparrow and an adult Microtus appeared in the same photograph. On one of these occurrences a song sparrow was battling its reflection when an adult, lactating Microtus came along the runway. The sparrow retreated about 12 inches toward the camera shelter and, as soon as the mouse had passed, returned to the runway. Brush rabbit.—All except four of the records of brush rabbits were in June and July of 1957, a season when these animals, especially young ones, were abundant. Figure 3 (below) shows that they were most active in the early morning. 30 a ge 20 Reo ies z = W z 3 = 10 ure SG Ti Ww x w 6 8 1012 2 4 6 8 10 12 2 4 6 JF MAMJIJ AS ON D NOON NIGHT Fic. 4.—Distribution by hours of 56 passages of shrews (left) and distribution by months of 56 passages of shrews (right). Shrew.—The dry, weedy habitat chosen was not favorable for shrews, and they were near the minimum weight necessary to depress the treadle of one of the recorders, so that some may have passed along the runway without making a record. The shrews were highly nocturnal (Fig. 4, left) and avoided the surface runways during the dry summer months (Fig. 4, right). Since captive specimens of Sorex are rarely inactive for more than one hour ( Morrison, Amer. Midl. Nat., 57: 493, 1957), the scarcity of records in the daytime probably means only that the shrews were not moving above ground at this time. They may have been foraging along gopher, mole and Microtus tunnels during the daytime. 376 178 JOURNAL OF MAMMALOGY Vol. 40, No. 2 A shrew was marked on March 4, a few inches from one of the recorders. It was captured 15 feet away on May 30 and 5 feet farther away on June 23. It passed along the study runway five times in the 16-week interval between first and last capture: on March 18, 27, 31, and April 17, and possibly on April 10 (markings obscured). Another shrew was recorded on March 27. Unless baited traps attract shrews from a considerable distance, or the recorder repels them, a trapper setting traps in this runway for a few nights would have had small chance of recording the presence of this individual which apparently was nearby for at least 16 weeks. Not a single shrew was recorded during the dry summer months of June, July and August. Nevertheless, on July 8 when I was checking the photo- electric recorder at 5:55 am, a shrew emerged completely from a small hole in fe) 90 ee e 3s ee Seee00e e eee 80 70 60 (%) 50 40 RELATIVE HUMIDITY 30 @® = SHREWS oO = LIZARDS 20 30 40 50 60 70 80 90 100 110 TEMPERATURE (oF) Fic. 5.—A comparison of the temperatures and humidities encountered by shrews and fence lizards in the runways. The larger circles show the position of the mean for each species. The large polygon encloses the range of temperatures and humidities available to the animals during the study. 377 May, 1959 PEARSON—TRAFFIC SURVEY 179 the ground a few inches from the instrument shelter, twitched his nose rapidly for a few seconds, and retreated down the same hole. The air temperature was 54° and the relative humidity 78 per cent—normal for this season. Obviously shrews were present on the study area during some or all of the summer months but were not frequenting the surface runways. Figure 5 shows the temperatures and relative humidities encountered above ground by the shrews on the study area compared with the total range of temperatures and humidities recorded throughout the study. By their nocturnal, winter-time activity shrews encountered the coldest, most humid conditions available in the region. In contrast, the similarly small, insectivorous fence lizards existing in the same habitat managed by their own behavioral patterns to encounter a totally different climate (Fig. 5). The mean of the temperatures recorded at the times of lizard passages was 39° warmer than that recorded for shrew passages, and relative humidity was 36 per cent lower. This activity pattern of shrews differs from that reported by Clothier iene. Mamm., 36: 214-226, 1955) for Sorex vagrans in Montana. He found shrews there to be active “both day and night and throughout the year, even during extremely bad weather.” It is important to understand, however, that he collected in damp areas near water, where the shrews may not have had to modify their activity to avoid desiccation. Extremely bad weather, for a shrew, is hot dry weather. Peromyscus.—Peromyscus truei was abundant in brushy places and in houses nearby; P. maniculatus was scarce. Some of the Peromyscus records were clearly of truei and some may have been of maniculatus, but many could not be identified with certainty. No adult P. californicus was recognized although a few young ones may have passed and been listed as truei. All passages of Peromyscus were at night. Salamander.—The record includes passages by both Ensatina escholtzii and Aneides lugubris. They were recorded in October, November, March and April. By being nocturnal and by avoiding the dry season, they encountered in these autumn and spring months about the same microclimate as shrews, but were recorded neither in the winter months nor at temperatures below 39°. A third species, Batrachoceps attenuatus, was common in the study area but is so small that it could not be expected to actuate either of the recorders. One Batrachoceps electrocuted itself underneath the treadle but has not been included in the records. Comparison of traps and recorders—The combination of live-trapping and photographing revealed a failure of small mammals to move between runways only a few feet apart. On several occasions meadow mice and harvest mice were live-trapped a few feet from one of the recorders, were released at the same place, and were recaptured a week or more later not more than a few feet away, yet during the intervening time they failed to pass the recorder. Conversely, some individual mice repeatedly recorded themselves on the films yet could never be induced to enter any of a large number of live traps placed 378 180 JOURNAL OF MAMMALOGY Vol. 40, No. 2 in the same runway and in nearby runways. It is obvious that all mice present do not use all of the active runways close to their home, and it is also obvious that neither the recorders nor traps give a complete accounting of the mice present. SUMMARY A motion-picture camera synchronized to an electronic flash unit was used to record the passage of animals along meadow-mouse runways and to record the temperature, relative humidity and time at which they passed. More than 26 species used the runways during 111 weeks of recording. Meadow mice, harvest mice, sparrows, brush rabbits and shrews passed most frequently. The average traffic per day in each runway was 11 passages; on some days there were more than 60 passages. Rarely more than ten meadow mice or six harvest mice used a runway in any one period. Meadow mice and harvest mice used the same runways simultaneously. Traffic by harvest mice alone did not keep the run- ways open. Meadow mice were active during the day and night; harvest mice were strongly nocturnal. Brush rabbits were active primarily early in the morning. Almost all shrews were recorded at night and in the winter months. Consequently, they encountered the coldest, most humid conditions available to them. In contrast, the similarly small, insectivorous fence lizards encountered a microclimate that was 39° warmer and 36 per cent less humid. Neither traps nor recorders accounted for all the individuals living nearby. Museum of Vertebrate Zoology, Berkeley, California. Received October 29, 1957. 379 PREY SELECTION AND HUNTING BEHAVIOR OF THE AFRICAN WILD DOG’ RICHARD D. ESTES, Division of Biological Sciences, Cornell University, Ithaca, New York JOHN GODDARD, Game Biologist, Ngorongoro Conservation Area, Tanzania Abstract: African wild dog (Lycaon pictus) predation was observed in Ngorongoro Crater, Tanzania, between September, 1964, and July, 1965, when packs were in residence. The original pack of 21 dogs remained only 4 months, but 7 and then 6 members of the group reappeared in the Crater at irregular intervals. The ratio of males:females was disproportionately high, and the single bitch in the small pack had a litter of 9 in which there was only one female. The pack functions primarily as a hunting unit, cooperating closely in killing and mutual defense, subordinating individual to group activity, with strong discipline during the chase and unusually amicable relations between members. A regular leader se- lected and ran down the prey, but there was no other sign of a rank hierarchy. Fights are very rare. A Greeting ceremony based on infantile begging functions to promote pack harmony, and appeasement behavior substitutes for aggression when dogs are competing over meat. Wild dogs hunt primarily by sight and by daylight. The pack often approaches herds of prey within several hundred yards, but the particular quarry is selected only after the chase begins. They do not run in relays as commonly sup- posed. The leader can overtake the fleetest game usually within 2 miles. While the others lag behind, one or two dogs maintain intervals of 100 yards or more behind the leader, in positions to intercept the quarry if it circles or begins to dodge. As soon as small prey is caught, the pack pulls it apart; large game is worried from the rear until it falls from exhaustion and shock. Of 50 kills observed, Thomson’s gazelles (Gazella thomsonii) made up 54 percent, newborn and juvenile wildebeest (Connochaetes taurinus) 36 percent, Grant’s gazelles (Gazella granti) 8 percent, and kongoni (Alcelaphus buselaphus cokei) 2 percent. The dogs hunted regularly in early morning and late afternoon, with a success rate per chase of over 85 percent and a mean time of only 25 minutes between starting an activity cycle to capturing prey. Both large and small packs generally killed in each hunting cycle, so large packs make more efficient use of their prey resource. Reactions of prey species depend on the behavior of the wild dogs, and disturbance to game was far less than has been represented. Adult wildebeest and zebra (Equus burchelli) showed little fear of the dogs. Territorial male Thomson’s gazelles, which made up 67 percent of the kills of this species, and females with concealed fawns, were most vulnerable. The spotted hyena (Crocuta crocuta) is a serious competitor capable of driving small packs from their kills. A minimum of 4-6 dogs is needed to function effectively as a pack. It is concluded that the wild dog is not the most wantonly destructive and disruptive African predator, that it is an interesting, valuable species now possibly endangered, and should be strictly protected, particularly where the small and medium-sized antelopes have increased at an alarming rate. The habits of the African wild dog or Cape hunting dog (Lycaon pictus) have been described, sometimes luridly, in most books about African wildlife. Accounts by such famous hunters and naturalists as Selous (1881), Vaughan-Kirby (1899), and Percival (1924), repeated and embellished by other authors, have created the popular image of a wanton killer, more destructive and disruptive to game than any other African predator. ‘Field work supported by the National Geo- graphic Society; also by grants from the New York Explorers Club and the Tanzania Ministry of Agriculture, Forests and Wild Life. 52 Because of its bad reputation, the wild dog was relentlessly destroyed in African parks and game reserves for many years. In Kruger National Park, for instance, it was shot on sight from early in the present century up until 1930 as part of an overall policy to keep predators down. In Rhode- sias Wankie National Park some 300 wild dogs were killed by gun and poison be- tween 1930 and 1958. Acceptance of modem concepts of wild- life management has finally brought an end to the indiscriminate destruction of wild dogs and other predators in most, if not all, African national parks. There is now 380 THE AFRICAN WiLpD Doc ° Estes and Goddard 53 a general awareness among game wardens of the predator's role in regulating popula- tions, which perhaps began with Stevenson- Hamilton (1947), Warden of Kruger Park for almost 30 years, who related the alarm- ing increase of impala (Aepyceros me- lampus) to the disappearance of the park’s formerly large wild dog packs. While the wild dog has benefited from more enlightened concepts of game man- agement, its reputation, still based on pop- ular writings and myth, remains unchanged. But recent scientific investigations indicate that a new and less-prejudiced evaluation of this species is long overdue. Kiihme (1965) has studied the social behavior and family life at the den of a pack with young whelps on the Serengeti Plains, Tanzania. We have observed prey selection and hunt- ing behavior in a free-ranging pack of adults and juveniles in nearby Ngorongoro Crater, a caldera with a floor area of 104 square miles that supports a resident pop- ulation of around 25,000 common plains herbivores. The two studies together throw quite a different light on the habits, char- acter, and predator-prey relationships of this highly interesting species. We are indebted to Dr. B. Foster of the Royal College, Nairobi, and to G. C. Roberts of the Crater Lodge for reporting four kills and one kill respectively, that they witnessed in the Crater; also to Pro- fessors W. C. Dilger, O. H. Hewitt, and H. E. Evans of Cornell University for criti- cal readings of the manuscript. Nomencla- ture follows Haltenorth (1963) for artio- dactyls, and Mackworth-Praed and Grant (1957) for birds. METHODS Most observations were made from a vehicle; we each had a Land Rover and usually operated independently. The wild dogs, like many other African predators in sanctuaries, paid very little attention to cars and could be watched undisturbed from within 30 yards or less. It was also feasible to keep pace with the pack during chases over the central Crater floor, either driving parallel to the leader at a distance of 100-200 yards or following behind and to one side so as not to get in the way of other pack members. To locate the pack initially, we often drove to an observation point on a hill and scanned the Crater with binoculars and a 20-power binocular tele- scope. When the pack was moving it could often be spotted at a distance of over 5 miles, and a number of chases and kills were clearly observed from a _ hilltop through the telescope. RESULTS Pack Composition The pack that first entered Ngorongoro Crater in September, 1964, contained 21 animals, including 8 adult males, 4 adult females, and 9 juveniles. They remained more or less continually in residence through December, then disappeared and were pre- sumed to have left the Crater. One juvenile female had died of unknown causes. Dur- ing January, 1965, seven members of the same pack, 4 males, 1 female, and 2 juvenile males, reappeared; after a lapse of 5 months, apparently the same animals, minus one male, again took up residence, and have been observed off and on up to the present writing. In March, 1966, the female whelped but died 5 weeks later, leaving 8 male and 1 female pups. They were brought up by the 5 males, who fed them by regurgitation until they were old enough to run with the pack. However, the female and 4 male pups died, leaving an all-male pack of 9 in August, 1966. While an all-male pack must be excep- tional, there is other evidence to suggest 381 54 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 that a high proportion of males may be common in this species. The pack Kihme studied consisted of 6 adult males and 2 adult females, which had 11 and 4 pups respectively, sex unreported. During 2-3 years of shooting in Kruger National Park, the ratio of males was 6:4, despite an attempt to select females (Stevenson-Hamil- ton 1947). We have no explanation to offer for the discrepancy, but if it is real and not normal, it might help explain the reported decline of wild dogs during recent years in many parts of Africa. Social Organization Leadership and Rank Hierarchy.—In the full pack of 21 and in the pack of 7, the same adult male was consistently the leader; he usually led the pack on the hunt, selected the prey, and ran it down. In the pack of 6, from which the above male was absent, the adult female was the leader. One of the males filled the position after her death. Apart from the position of leader, we saw no indication of a rank order. Kihme con- cluded there was no hierarchy in the pack he observed, nor even a leader. The equality of pack members may partly explain the singularly amicable relations typical of the species. On the other hand, competition for food and females could easily lead to ag- gression; yet neither Kuhme nor we ever saw a fight. Food Solicitation and Appeasement Be- havior.—Overt aggression and fighting are minimized through ritualized appeasement behavior derived from infantile food beg- ging. Begging and appeasement appear in almost every contact between individuals, and particularly in situations where aggres- sion would be most likely to occur—for instance, when animals are competing over a kill. However, we cannot comment on sexual competition, having seen none; we observed sexual behavior on only two oc- casions, when one male mounted another repeatedly as the latter was feeding at a kill. Kihme also saw very little sexual be- havior. When two animals were competing for the same piece of meat, each would try to burrow beneath the other, its forequarters and head flat to the ground and _hind- quarters raised, tail arched and sometimes wagging. The ears were flattened to the head and the lips drawn back in a “grin,” while each gave excited twittering calls. As Kithme observed (p. 516), the dogs “tried to outdo each other in submissiveness.” In this way juveniles and even subadults manage to monopolize kills in competition with adults. The young thus enjoy a priv- ileged position in the pack. Pups at the den successfully solicit any adult to regur- gitate food by poking their noses into the corner of the adult’s mouth, sometimes lick- ing and even biting at the lips. Since all pack members contribute to feeding and protection of the young, the mother is not essential to their survival after the first few weeks. Greeting Ceremony.—Whenever the pack became active after a rest period, and particularly if two parts of the pack were reunited after being separated, the mem- bers engaged in a Greeting ceremony ( Fig. 1), in which face-licking and poking the nose into the corner of the mouth played a prominent part. The ceremony thus ap- pears to be ritualized food solicitation; the fact that Kihme actually saw regurgitation elicited by begging adults supports this in- terpretation. The Greeting ceremony in the wolf (Canis lupus), in which one takes another’s face in its jaws, may have the same derivation. As a prelude to greeting, dogs typically adopted the Stalking attitude (Fig. 2), with the head and neck held horizontally, shoul- ders and back hunched, and the tail usually 382 THE AFRICAN WILD Doc « Estes and Goddard 55 Fig. 1. Greeting ceremony. hanging. Kihme (p. 512) interprets this posture as inhibited aggression; the same attitude is adopted when approaching po- tential prey and competitors of other species. The Stalking posture changed to greeting when dogs got close. In greeting- solicitation, as they licked each other’s lips and poked the nose into the corner of the mouth, one or both crouched low, with head, rump, and tail raised stiffly (Fig. 1). Except for the raised head, this resembles the submissive posture displayed when two dogs are competing over food. The Greet- ing ceremony was also frequently per- formed while two dogs trotted or ran side by side. Vocal Communication.—Although Perci- val (1924), Stevenson-Hamilton (1947), Ma- berly (1962), Kiihme (1965), and others have given good descriptions of wild dog calls, the function of the calls has often been misinterpreted. This applies partic- ularly to two of the three most frequently heard calls (Nos. 1 and 3): 1. Contact call—a_ repeated, bell-like “hoo.” Often called the Hunting call, it has nothing to do with hunting as such, but is given only when members of a pack are separated. Though a soft and musical sound, it carries well for 2 or more miles. When members of the Ngorongoro pack were missing, an imitation of the Contact call would bring the rest to their feet, whereas there was at best only a mild reac- Fig. 2. The Stalking attitude, here displayed by the pack leader while approaching a herd of gazelles. tion to imitations when the full pack was assembled. 2. Alarm bark—a deep, gruff bark, often combined with growling, given when star- tled or frightened. A good imitation near a resting pack elicited an immediate star- tled reaction. 3. Twittering—a high-pitched, birdlike twitter or chatter. The most characteristic and unusual vocalization, it expresses a high level of excitement. It is given in the prelude to the hunt, while making a kill, in mobbing hyenas or a pack member, and by dogs competing over food. Its primary function is evidently to stimulate and con- cert pack action. Kuhme described this call (Schnattern) only in the context of the Greeting ceremony (p. 513). Besides these vocalizations, whining may be heard during appeasement behavior and when pups are begging, and members of the pack sometimes yelp like hounds when close on the heels of their prey. Kiihme (p. 500) further distinguishes an Enticing call (Locken) given by adults calling the young out of the den, and a Lamenting call (Klage) given by pups when deserted. Olfactory and Visual Communication.— Wild dogs hunt primarily by sight and by daylight. We never saw them track prey by scent. Though they evidently have a good nose and may well use it for tracking in bush country, olfaction in this species seems to havea primarily intraspecific significance. 383 56 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 ao ° gE (Cp) +O =! le = oO we Le Lo & ree END 2 ie : ey eho foil 2 1 eS "Aes 76 A.M. PM Th ME Fig. 3. Time distribution of 50 wild dog kills. Wild dogs are renowned for their peculiarly strong, and to many humans disgusting, odor, which may emanate from anal glands but seems to come from the whole body. Sniffing under the tail, responsive urination and defecation are socially important activ- ities. But the main role of the strong body odor may be to permit high-speed tracking of the pack by members that have lost visual contact. Lagging members seen run- ning on the track taken by the rest of the pack sometimes appeared to be using their noses. Similarly, the white tail tip probably helps maintain visual contact in bush coun- try, high grass, and under crepuscular con- ditions; in a species notable for every pos- sible color variation, a white-tipped tail is the most constant and conspicuous mark. Daily Activity Pattern The Ngorongoro pack had two well-de- fined hunting periods each day (Fig. 3). That this periodicity is characteristic of the species may be inferred from Kihme’s ob- servations (p. 511), and from Stevenson- Hamilton’s (1947) observations in Kruger National Park. In nine recorded instances, though, the Ngorongoro dogs killed between 8:30 am and 3:30 pM, well outside the nor- mal periods. Failure to kill during the regular hunting cycle is the likeliest ex- planation; it was more usual, however, for the pack then to wait until the following regular period. Wild dogs will also hunt on moonlight nights, as Stevenson-Hamilton noted. When the Crater dogs had not killed before dusk, the hunt was sometimes pro- longed. The latest kill we recorded was at 7:32 pM, when it was fully dark. Since they are capable of functioning as a pack and of hunting successfully after dark, the fact that wild dogs are so strongly diurnal may seem puzzling. But it may be explained by the fact that they hunt mainly by sight; it would be much more difficult to locate prey and single out a quarry at night. As to the regularity and brevity of their hunting cycles in early morning and late afternoon, this is partly a measure of their hunting efficiency, discussed below. Also, of course, these are the times in the day when diurmal animals, particularly herbivores, are most active and most ap- proachable. Apart from a certain amount of play and other social activities shortly before starting to hunt and immediately after feeding, pack members were usually active only while actually hunting. At other times they could often be found resting near or in the same place where they had settled after the morming or evening kill. When resting, pack members customarily lay touching in close groups (Fig. 4). Generally speaking, the pack became active between 5:30 and 6:15 pm, and in the morning within % hour of dawn, remaining active for 1-2 hours. But where game is less plentiful than it is in Ngorongoro, and a pack must range more widely (Stevenson-Hamilton gives a range of at least 1,500 square miles for a Transvaal pack whose movements were reported over a period of years), a good deal of time between and during hunts must be spent in travel. 384 THE AFRICAN WILD Doc « Estes and Goddard roe na : : ; ‘ x ¥e . f . : Of sof . Co i 2 s £ . aes *E Fig. 4. Part of a resting pack, lying typically close together. Hunting Behavior Prelude to the Hunt.—Periods of activity were initiated by the actions of one or a few dogs apparently more restless than the others; rarely did the whole pack arise spontaneously at the start of an activity cycle. Typically, one dog would get up and run to a nearby group, nose the others and tumble among them until they re- sponded. Within a few minutes the whole pack would usually become active. But if, as sometimes happened, the majority failed to respond to the urging of a few, then all would settle down to rest again. Sometimes, after a brief bout of general activity, the whole pack would lie down once more, even if it was past the usual time of hunt- ing. During the first 5 or 10 minutes after rousing, the pack members sniffed, urinated, defecated, greeted, and romped together. Play and chasing tended to become pro- gressively wilder and reached a climax when the whole pack milled together in a circle and gave the twittering call in unison. As soon as this melee broke up, the pack usually set off on the hunt. Kiihme (p. 522) interprets this performance (specifically the Greeting ceremony) as “a daily re- peated final rehearsal for the behavior at the kill,” wherein mutual dependence and friendliness are reinforced by symbolic beg- ging, thus enabling the dogs to share the kill amicably. While this may be one func- tion, the progressive buildup of excitement before hunting looked to us like nothing so 57 much as a “pep rally,” that served to bring the whole pack to hunting pitch. The be- havior of domestic dogs urging one another to set off on a chase is somewhat similar. The Mobbing Response.—During the mill- ing preparatory to hunting, we sometimes saw what appeared to be incipient mob- bing action toward a pack member, when up to half a dozen dogs would gang up on one, tumble and roll it but without actually biting it. Intensive play between two or three animals usually preceded and seemed to trigger a mobbing reaction in other mem- bers, who signaled their intentions by ap- proaching in the Stalking posture. Percival (1924:48) reports seeing a pack mob and kill a wild dog he had wounded. The oc- currence of “play” mobbing suggests that it could indeed become serious when an animal is maimed. On the other hand, sick and crippled pack members are often not molested: one very sick-looking old male in the large pack trailed behind the others for over a month before recovering, and though he kept usually a little apart, was tolerated at kills. It is significant that basically the same mobbing behavior, at high intensity, is dis- played when wild dogs kill large prey and when they harass spotted hyenas, their most serious competitor. It seems very likely, in fact, that mobbing is an innate re- sponse which governs pack action in hunt- ing, killing, and mutual defense. It is per- haps the key to pack behavior in all animals that display it. That mobbing appears in 385 58 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 play and can be released by a conspecific which is wounded or otherwise transformed from its normal self, supports the hypothesis that it is an innate response. It is also note- worthy that a wild dog removed from its pack apparently makes little effort to defend itself against attack. Selous (in Bryden 1936:24) reported that a wild dog caught by a pack of hounds shammed death and then escaped when he was about to skin it. Hunting Technique.—Sometimes the pack would set off on the hunt at a run and chase the first suitable prey that was sighted. More often, there was an inter- val of 10-20 minutes during which the dogs trotted along, played together, and engaged in individual exploratory activity, stopping to sniff at a hole or a tuft of grass, then running to catch up with the rest. At this stage, when the hunt had started but before any common objective had been deter- mined, individuals might forage for them- selves. The observer would suddenly notice that a dog was carrying part of a gazelle fawn or a young hare (Lepus capensis), that must have been simply grabbed as it lay in concealment. Once during a moon- light hunt by a small pack that visited the Crater in 1963, individual dogs were seen to pick up at least two gazelle fawns and one springhare (Pedetes surdaster), a strictly nocturnal rodent, within % hour. Concealed small game such as this is ap- parently not hunted by the pack in concert. Preparatory to the chase, there was fre- quently a preliminary stalking phase dur- ing which the pack approached herds of game at a deliberate walk, in the Stalking attitude (Fig. 2). The dogs appeared to be attempting to get as close as possible with- out alarming the game, and certainly the flight distances were much less than when the pack appeared running. The chase was launched the moment the game broke into flight. But game that began running at more than 300 yards was generally not pursued. As far as we could tell, the prey animal was never singled out until after the pack, or at any rate the leader(s), had broken into a run. In the pack of 21, juveniles and some adults usually lagged far behind, and often caught up 5-10 minutes after the kill was made. In the small pack, however, com- monly all kept together and spread out on a front during the stalking phase. When all started running on a front, sometimes more than one dog picked out a quarry from the fleeing herd, whereupon the pack might split, some following one dog, the rest another. Kihme (p. 527) considered this the normal pattern and noted that often each animal acted for itself in selecting a quarry before all combined on a common goal. In this way the slowest prey tended to be selected. Selection by this method was exceptional for the Ngorongoro pack, which had a definite leader; as a rule the lead dog made the choice and the rest of the pack fell in behind him. Nor did it appear that any effort was made to single out the slowest prey, although that would be difficult to observe clearly. Again as a general rule, no attempt was made to carry out a concealed stalk, which would in any case be practically impossible by daylight on the short-grass steppe. But on one occasion the pack of six made use of a tall stand of grass to get near a group of Thomson’s ‘gazelles. On another hunt the pack apparently took advantage of a slight elevation in the expectation of surprising any game that might be out of sight on the far side. They moved deliberately up the slope, then broke into a run and swept at full speed over the crest on a broad front —but without finding any quarry that time. When the leader had selected one of a fleeing herd, he immediately set out to run it down, usually backed up by one or two 386 THE AFRICAN Wi1LD Doc « Estes and Goddard 59 other adults who maintained intervals of 100 yards or more behind him, but might be left much further behind in a long chase. The rest of the pack lagged up to a mile in the rear. Discipline during the chase was so remarkable among all pack members that even gazelles which bounded right be- tween them and the quarry were generally ignored. The average chase lasted 3-5 minutes and covered 1-2 miles. At top speed a wild dog can perhaps exceed 35 mph, and can sustain a pace of about 30 mph for several miles. Once when a chase had begun but no single quarry had yet been selected, a male in the pack of 21 broke away and proceeded to make a 5- mile circular sweep quite by itself, turning on bursts of speed when gazelles bounded off before him, but without ever singling one out. His average speed, as determined by pacing him in a vehicle, was approxi- mately 20 mph. In descriptions of wild dog hunting methods, much has been made of their intelligent cooperation in “cutting comers” on their prey, and particularly of their relay running, with fresh dogs taking the place of tired leaders. We concur that there is a basis for the first idea, but we saw no evi- dence whatever to support the contention that wild dogs run in relays. The truth is that wild dogs have no need to hunt in relays. The lead dog has ample endurance, if not the speed, to overtake probably any antelope, of which gazelles are among the fleetest. The fact that other members of the pack are able to cut corners on the prey is at least partly accounted for by the prey’s tendency to circle instead of fleeing in a straight line. As explained later, some prey animals have a greater tendency than others of their species to do this. Of course, once overtaken, even a quarry that has been running straight is forced to start dodging if it is to avoid being caught straightaway. Thus a dog running not too far behind the leader is well placed to cut corners when the quarry changes course, and it frequently happened that one of the followers made the capture. Most game, after a hard chase of a mile or two, was too exhausted by the time it began dodging to have any real chance of evading its pursuers. Killing and Eating—Wild dogs killed small game like Thomson’s gazelles with amazing dispatch. Once overtaken, a gazelle was either thrown to the ground or simply bowled over, whereupon all nearby dogs fell on it instantly. Grabbing it from all sides and pulling against one another so strongly that the body was suspended between them, they then literally tore it apart (Fig.5). It happened so quickly that it was never possible to come up to a kill before the prey had been dismembered. If it didn’t go down at once, dogs began tear- ing out chunks while it was still struggling on its feet. We once saw a three-quarter term fetus torn from a Thomson’s gazelle within seconds of the time it was overtaken and before it went down. As Kihme ob- served, there is no specific killing bite as in felids (Leyhausen 1965). When dealing with larger prey such as juvenile wildebeest and notably a female kongoni, the dogs slashed and tore at the hind legs, flanks, and belly—always from the rear and never from in front—until the animal fell from sheer exhaustion and shock. They then very often began eating it alive while it was still sitting up (Fig. 6). Self-defense on the part of a prey was never once observed; the kongoni, for example, did little more than stand with head high while the dogs cut it to ribbons, looking less the victim than the witness of its own execution. In eating, the dogs began in the stomach cavity, after first opening up the belly, and proceeded from inside out. Entrance was 387 60 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 Fig. 5. The pack tearing apart a young gnu calf. also effected through the anus by animals unable to win a place in the stomach cavity. While several dogs forced their heads in- side and ripped out the internal organs, others quickly enlarged the opening in struggling for position. This resulted in skinning out the carcass, leaving the skin still attached to the head, which was sel- dom touched. Apart from these, the back- bone and the leg bones, very little of a Thomson’s gazelle would remain at the end of 10 minutes. In the pack of 21, if only part had managed to eat their fill, sometimes the rest went off to hunt again before the carcass was cleaned. They pro- ceeded to chase and pull down another gazelle within as little as 5 minutes from the time of the previous kill, to be joined shortly by the other dogs. As each animal became satisfied it withdrew a little from the kill and joined others to rest, play, or gnaw at a bone it had taken along. Some- times the pack stayed at the scene until the next hunting period; more often it with- drew to a nearby stream or waterhole and settled down there. Kiihme never saw wild dogs drink. The Ngorongoro pack drank, though irregularly, before hunting and after eating. 388 Selection of Prey and Frequency of Kills Table 1 summarizes prey selection by species, sex, and age in 50 recorded kills. The 11 wildebeest calves were all taken in January during the peak calving season, when the pack of seven dogs apparently specialized on them; only kills of calves were seen by us or reported by Crater visi- tors in this month. Thus the percentage of calves in the total gives a biased picture of prey selection during the rest of the year. With new calves excluded, the adjusted percentages, based on 39 kills, are as fol- lows: Thomson’s gazelles 69 percent Juvenile wildebeest 18 percent Grant’s gazelles 10 percent Kongoni one kill Wright (1960:9) records a similar pre- ponderance of Thomson’s gazelles in 10 ” oa ee fe a oe Figs 6: still alive, but evidently in a state of deep shock. Dogs begin eating a yearling-class gnu while it is Tue AFRICAN WILD Doc ° Estes and Goddard 6 ADULT JUVENILE-— PERCENT OF FEMALES SUBADULT Younc* ToTaL KILLs 6 2 1 54 0 ff ll 36 1 2 0 8 1 0 0 2 Table 1. Prey selection by species, sex, and age in 50 kills of the African wild dog. PREY TorTaL ADULT SPECIES No. MALES Thomson’s gazelle 27 18 Wildebeest 18 0 Grant’s gazelle 4 1 Kongoni il 0 * Less than 6 months old. kills on the Serengeti Plains (7 Thomson’s gazelles, 1 wildebeest, 1 impala, and 1 reed- buck [Redunca redunca]), and notes that it is the staple diet of wild dogs in the Serengeti. Kiihme also observed that wild dogs prey mainly on Gazella thomsonii and G. granti, and young wildebeest in the Serengeti. In terms of actual preference, informa- tion from the Serengeti, where the Thom- son’s gazelle is by far the most numerous herbivore, is far less revealing than the fig- ures from the Crater, where this species oc- curs in relatively small numbers. The status of the principal ungulates in Ngorongoro, based on an aerial count by Turner and Watson (1964), on two ground counts of the gazelles by the authors in collaboration with the Mweka College of Wildlife Man- agement, and on our ground counts of the less numerous species, is as follows: Wildebeest 14,000 Zebra 5,000 Thomson’s gazelle 3,500 Grant’s gazelle 1,500 Eland (Taurotragus oryx) 350 Waterbuck (Kobus defassa) 150 Kongoni 100 Reedbuck 100 (?) The evidence suggests, then, that Thom- son’s gazelle is the preferred prey of the wild dog in East African steppe-savanna. In the miambo woodland (Brown 1965) that extends from mid-Tanzania into South Africa, where gazelles are not found, the main prey may be impala, followed by other medium- to small-sized antelopes and the young of large antelopes. In Kruger Park, for example, of 88 identified wild dog kills, 85 percent were impala (Bourliere 1963). Stevenson-Hamilton listed other prey as reedbuck, bushbuck (Tragelaphus scrip- tus), duiker (Sylvicapra grimmia and Cephal- ophus spp.), and steinbok (Raphicerus campestris), also female waterbuck and kudu (Tragelaphus strepsiceros) when pressed by hunger. In Wankie Park, war- dens’ reports indicate a considerable toll of young kudu, eland, sable (Hippotragus niger), and tsessebe (Damaliscus lunatus). Instances where adult female and even adult male kudu were pulled down by wild dogs are also cited. Bourliere states (1963:21) that “Carnivores actually only prey upon herbivores of about the same size and weight.” While this gen- eralization is open to dispute, it applies well enough to East African wild dogs preying on Thomson’s gazelles. Where the main prey is impala, reedbuck, etc. that weigh in the 100-150 Ib class, weight and size may be double or triple that of the wild dog. But the wild dogs of the East African steppe-savanna are smaller (also darker, with more black and less tan and white) than their counterparts in Central and South African woodland (Fig. 7). The average weight of the animals we have seen in East Africa would not exceed 40 lb; the members of a pack seen in Wankie Park, by comparison, looked to be a good 3 inches taller and 20 lb heavier. This consistent geographic size variation may be adapted to size of the principal prey species; specifi- 389 62 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 Fig. 7. cally, wild dogs of the East African plains may be smaller as the result of specializa- tion on Thomson’s gazelle. Kill Frequency.—Because of the difficulty of locating and relocating a free-ranging pack, our data for consecutive hunting periods are inadequate for defining the aver- age kill frequency and average food intake per animal per day. Even when the pack was observed during the two daily hunting periods, it was rarely certain that it had not killed before, after, or between these periods. Nonetheless, because this type of information is badly needed, data covering consecutive hunting periods are presented in Table 2 as a rough average of kill fre- quency and meat available per animal per day. The average frequency of two kills per day derived from the data for consecutive hunting periods agrees with our general ob- servation that the pack usually killed dur- ing each period. To demonstrate this, on 28 hunts the pack performed as follows: Chases Kills Failures Did not chase 29 25 4 5 This indicates a success rate per chase of over 85 percent. As a further indication of efficiency in locating and running down Two specimens of the larger, lighter-colored wild dog of southern Africa, photographed in Wankie National Park. prey where game is plentiful, on eight oc- casions when the dogs were watched from the moment they left their resting place to the moment they killed, the mean time was only 25 minutes, with a range of 15-45 min- utes. On five other occasions the pack failed to hunt seriously during the normal period; this was offset in the above figures by five periods during which the dogs chased and killed twice. The possibility that hunting activity and success might be reduced after having killed larger or more than one of the usual prey is not borne out by the six instances when the pack was ob- served during the next hunting period: in four cases the pack killed again. There are some grounds for asserting, then, that wild dogs kill twice daily regardless of what their prey may be. Certainly they do not feed more than once from the same kill, at least not in Ngorongoro Crater, where the numerous scavengers dispose of all left- overs in very short order. Meat Available per Animal per Day.— The amount of meat available per wild dog per day works out at roughly 6 lb, assuming that 40 percent of the prey animal consists of inedible or unpalatable bone, skin, and stomach contents. Wright’s (1960) calcula- tion of 0.15 lb of food per day per pound 390 Tue AFRICAN WILD Doc * Estes and Goddard 63 Table 2. Kill frequency and meat available per dog per day, based on observations of consecutive hunting cycles. AVAIL- Est. Wt. No. In ABLE* MEAT/ DATE PREY (LB) Pack MeEat/ Doc/Day Doc 1964 Sept. 30 Juvenile wildebeest 125 a1 3.6 3.6 Oct. 1 Thomson’s gazelle (adult M) 60 21 Wet " " (adult F) 40 PAL ial 2.8 Nov. 11 Thomson’s gazelle (adult F, including fetus) 50 21 1.4 2 Thomson’s gazelles (adult F) 80 21 2.2 26 Nov. 12 Thomson’s gazelle (adult M) 60 21 Nef Kongoni (adult F) 250 21 7.4 9.1 Nov. 27 2 Thomson’s gazelles (adult M) 120 il 3.4 Thomson’s gazelle (subadult M) 50 ot 1.4 4.8 Nov. 28 Grant’s gazelle (subadult F) 90 oH 2.6 Thomson’s gazelle (adult M) 60 PM a Bye 4.3 Dec. 5 (PM) 2 Thomson’s gazelles (adult M) 120 12 6.0 to Dec. 7 (AM) Thomson’s gazelle (juv. M) 40 21 1.1 eo 1965 Jan. 17 (PM) 4 wildebeest calves 180 c 15.5 7.8 to Jan. 19 (am) July 16 2 Thomson’s gazelles (adult M) 120 6 12.0 12.0 Kill frequency = 2 kills/day. Meat available per dog per day: combined average = 6 lb; for pack of 21 = 4.5 lb; for pack of 7-6 = 9 Ib. * Available meat is based on 60 percent of carcass weight. of dog also works out to 6 lb per day if the average weight of a dog is taken as 40 |b, but his figures are based on the total weight of the prey. In either case, two to three times as much food per day is avail- able to wild dogs as is given to domesti- cated dogs of the same size. However, the number of dogs in the pack is an important factor. When there were 21 dogs, the amount of meat available per day was less than 5 lb per animal; in the pack of 7 and 6, each animal had approximately twice as much available meat. Since the small packs killed at the same rate, large packs are un- doubtedly less wasteful. Reactions of Prey Species The reactions of game depended on the behavior of the wild dog pack. When the pack was at rest, all game would graze un- concernedly within 150 yards. When the dogs were walking or trotting, potential prey would stand until approached within 350-250 yards, or less if the pack was not headed directly toward them. When stalked, gazelles often stood watching until the pack came within 300-200 yards. But when the pack was running, gazelles, and wildebeest herds containing young, often acted alarmed at a distance of 500 yards, although again, individual animals not directly in the ap- proach line might let the pack go by as close as 150 yards. Gazelles—The moment a running wild dog pack appeared on the plain, both ga- zelle species immediately reacted by per- forming the stiff-legged bounding display, with tail raised and white rump patch flash- ing, called Stotting or Pronking. Un- doubtedly a warning signal, it spread wave- like in advance of the pack. Apparently in response to the Stotting, practically every 391 64 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 gazelle in sight fled the immediate vicinity. Adaptive as the warning display may seem, it nonetheless appears to have its drawbacks; for even after being singled out by the pack, every gazelle began the run for its life by Stotting, and appeared to lose precious ground in the process. Many have argued that the Stotting gait is nearly or quite as fast as a gallop, at any rate decep- tively slow. But time and again we have watched the lead dog closing the gap until the quarry settled to its full running gait, when it was capable of making slightly bet- ter speed than its pursuer for the first half mile or so. It is therefore hard to see any advantage to the individual in Stotting when chased, since individuals that made no dis- play at all might be thought to have a bet- ter chance of surviving and reproducing. On theoretical grounds, then, it has to be assumed that the Stotting display offers an individual selective advantage which simply remains to be determined. Nor is this type of display confined to the gazelles: during the aforementioned kongoni chase, all six members of the herd began Stotting when the wild dog pack first headed in their di- rection, and the victim continued to Stot for some time after being singled out. Table 1 shows that 67 percent of the Thomson’s gazelles killed were adult males. This is evidently the result of territorial be- havior. Because of attachment to territory, probably coupled with inhibition about trespassing on the grounds of neighboring rivals, territorial males tend to be the last to flee from danger. Moreover they show a greater tendency to circle back toward home, and these two traits together make them more vulnerable to wild dog preda- tion than other members of the population. The same tendencies are displayed by fe- males with young, concealed fawns, making them also more vulnerable. Wildebeest—Adult wildebeest, espe- cially territorial bulls, show little fear of wild dogs, which is a good indication that they have little reason to fear them under normal circumstances (Fig. 8). While even territorial males will get out of the way of a running pack, they rarely leave their grounds, but merely trot to one side and turn to stare as the pack goes by. Bulls not infrequently act aggressively toward walk- ing or trotting dogs, and may even make a short charge if the dogs give ground. In Rhodesia we have seen a pack of the larger variety of wild dogs chased by females and yearlings of the blue wildebeest (C. t. taurinus ) which is also larger and perhaps generally more aggressive than the Western white-bearded gnu. But like zebras, all wildebeest will on occasion follow behind walking or trotting dogs, apparently moti- vated by curiosity, just as they will gather to stare at and follow lions (Panthera leo). In hunting wildebeest, wild dogs are ob- viously highly selective. Having walked in the Stalking attitude to within several hun- dred yards or less and then run into the midst of a large concentration, the pack splits up and works through it, approaching one gnu after another only to turn away if it proves adult. Meanwhile the wildebeest mill and run in all directions, without ever making any effort to form a defensive ring —even when young calves are present. A defensive ring has been reported in some of the wild dog literature. Kiihme (p. 528) observed something of the sort in large Serengeti concentrations, though they did not form any regular ring but simply crowded together in a milling mass. Indi- vidual females, on the other hand, defend their calves after being overtaken in flight. Against a pack, however, one wildebeest cannot put up any effective defense; while it confronts one or two, the rest go around and seize the calf. Zebra.—The only other herbivore whose 392 THE AFRICAN WILD Doc ° Estes and Goddard 65 Fig. 8. Adults, and even a yearling gnu (4th from left) show little fear of running wild dogs, though they ran out of the way immediately after the picture was taken. The quarry is a young calf, visible as a light spot in the upper left. reactions to wild dogs we observed in de- tail, zebras are the least concerned about them, and do not hesitate to attack dogs that come too close. Wild dogs on their part rarely stand up to them. Since the members of a harem would probably co- operate with the herd stallion to defend the foals, it would appear that wild-dog preda- tion on zebra is quite rare. Relations with Other Predators and Scavengers Vultures.—Since wild dogs customarily kill in early morning and late afternoon, the larger vultures, the white-backed (Pseu- dogyps africanus), Rippells griffon (Gyps riippelli), and lappet-faced (Torgos trache- liotus), whose activities are largely regu- lated by the presence or absence of thermal updrafts, benefit rather little from their pre- dation. Large vultures were more likely to appear at afternoon than morning kills. But the two smallest species, the hooded and Egyptian vultures (Necrosyrtes monachus and Neophron perenopterus), were regu- larly to be found at wild-dog kills, a good hour before other scavengers were even air- borne. In addition to these vultures, other regularly encountered scavengers included the tawny eagle (Aquila rapax) and the kite (Milvus migrans), while the uncom- mon white-headed vulture (Trigonoceps occipitalis), the bateleur eagle (Terathopius ecaudatus), and Cape rook (Corvus capen- sis) showed up infrequently. On several occasions hooded vultures were seen following a chase and landing before the prey had even been pulled down, shortly after full daylight. Aside from glean- ing bits and pieces around the kill, vultures had to wait until the dogs left before they could feed on the carcass. But the kite suc- cessfully stole small pieces from the dogs by swooping, grabbing, and mounting again to eat on the wing. Although young ani- mals sometimes stalked and ran at vultures 393 66 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 that approached close to the kill, the dogs were generally tolerant toward avian scav- engers. Jackals—The Asiatic jackal (Canis aureus) was seen more frequently at kills than the black-backed jackal (C. meso- melas). Since the latter seemed to predomi- nate at nocturnal kills by lions or hyenas, it may be that one is more nocturnal and one more diurnal in its habits. Also, the Asiatic jackal tended to behave more boldly and aggressively at kills. It would move closer to a feeding pack of dogs and take advantage of any opportunity to steal meat. When threatened by a dog, a little 15-lb jackal, coat fluffed, head down, and snarl- ing, would stand its ground and snap fero- ciously if the dog continued to advance. Although it was pure bluff that quickly ended in flight if a dog attacked in earnest, it proved a surprisingly effective intimida- tion display in most encounters. But on the whole, wild dogs behaved almost as toler- antly toward jackals as toward vultures. Spotted Hyenas.—Spotted hyenas, on the other hand, seriously compete with the dogs for their kills, attempting to play a commensal role against active resistance. In a place like the Crater, with an excep- tionally large hyena population for such a small area, numbering some 420 adults (Kruuk 1966:1258), it is probably safe to say that wild dogs hunting singly or in twos and threes would very frequently lose their kills to hyenas, since this happened oc- casionally even to the pack of 21. Hyenas actually stayed near the resting pack for hours at a time, evidently waiting for a hunt to begin. It was not unusual to see one or more of them slowly approach a group of dogs, then crawl to within a few yards and lie gazing at them intently, as though urging them to get started. Often several would wander between resting groups, sniffing the ground, consuming any stools they found, and coming dangerously close, to stand staring with their short tails twitching—a sign of nervousness. Kiihme (p. 534) reports an instance in which a hyena even touched a resting wild dog’s face, meanwhile “whining friendly.” Such boldness, particularly near the time when the pack was becoming active, often trig- gered the Mobbing response. Hyenas, which weigh up to 150 lb, would be more than a match for wild dogs if they had the same pack (mobbing) instinct. Lacking it, they are nearly defenseless against a wild dog pack. With three to a dozen dogs worrying its hindquarters, the best a hyena can do is to squat down and snap ineffectively over its shoulder, while voicing loud roars and growls. On rare oc- casions a hard-pressed one would simply lie down and give up; a hyena we once saw crowded by a persistently curious group of juvenile wildebeest did the same thing. The spotted hyena seems on the whole to be notably timid by nature, as may be judged from the fact that mothers will often not even defend their offspring. Yet they are driven by hunger to take incredible and sometimes fatal risks. Often, as under the above circumstances, they provoked attack by their own rash- ness. But in other cases the dogs seemed to go out of their way to harry hyenas en- countered during the early stages of a hunt. Those unwary enough to let the pack get close could still usually get off entirely by cowering down and lying still. But those that stayed until the pack was close and then ran away were inviting pursuit and a good mauling. At the same time, hyenas following behind the pack were generally ignored. On one notable occasion, the pack of 21 took it in turns to mob the hyenas it happened upon in a denning area inhabited by more than 30 adults and cubs, many of which were foregathered as usual prior 394 THE AFRICAN WILD Doc ° Estes and Goddard 67 to the evening foraging. What was most surprising was that none, on this or any other occasion, attempted to take refuge underground. When hard-pressed, even half-grown pups bolted into nearby dense streamside vegetation, where the dogs did not follow. But presumably young pups were hidden in the dens, since one lactating female was reluctant to quit the immediate vicinity. She was repeatedly mobbed. Set upon by five or six dogs at a time, she would maintain a squatting defense as long as she could bear it, then break free to race for the nearest hole. Instead of going down it or backing into it, she threw herself into cup-shaped depressions next to the holes, which may or may not have been excavated by the hyenas themselves (territorial wilde- beest also dig these depressions by pawing and horning the earth). In these she lay flat and tried to defend herself from the dogs, to whom only her back and head were ex- posed, while keeping up a steady volume of roars, growls, and staccato chuckles. Eventually she also took refuge in the bushes. Neither this hyena nor the next, which the dogs turned on its back and mauled for 2 minutes, bore any visible wounds. In fact, we have never known the dogs to kill or even seriously injure one. Either hyenas have exceedingly tough hides or else wild dogs are less in earnest about mobbing them than might appear. Yet the degree to which hyenas are able to capitalize on wild-dog predation for their own benefit would justify a deep antago- nism. They frequently drive away the last dogs on a kill unless the rest of the pack remains close by, and are quite capable of taking meat away from one or two dogs only a few yards removed from a kill where the rest are feeding. A more extraordinary example of this exploitation is the way hyenas take advantage of the wild dog’s hunting technique: in the final moments of Fe. 6: ing it alive, while one of two dogs that caught it looks on, panting heavily from the chase. half-grown. Hyenas appropriate a wild dog prey and begin eat- Hyena in foreground is As shown in Fig. 6, the dogs reclaimed their prey when the rest of the pack arrived. a chase, when only one or a few dogs are close to the quarry, hyenas have an oppor- tunity to appropriate it before the resi of the pack arrives (Fig. 9). They attempted this with considerable regularity in the Crater, and we succeeded in recording one instance on film. In some cases it was a matter of chance that hyenas were near enough the scene of the capture to dash in at the decisive moment; in others up to three or four actually took part in the chase from the beginning. Though not as fast as the dogs, they were able to be in a position to intercept the quarry if it doubled back, or to grab it away from the dog(s) as soon as it was caught. When only two or three of them were on hand, the dogs hesitated to launch an immediate counterattack, par- ticularly if more than one hyena was in- volved. But usually other pack members quickly appeared, joined together to mob the hyenas, and forced them to surrender the kill. But sometimes the dogs were defeated by sheer numbers. Once when the leader of the pack of 21 had pulled down a juve- nile wildebeest in a hyena denning area, 395 68 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 some 40 hyenas closed in on the kill before the others could gather. Apparently intimi- dated by so many competitors, the dogs re- venged themselves by mobbing stragglers, punishing them savagely. Twenty minutes later, while they were ranging for new prey, the hyenas pulled down an adult fe- male wildebeest on their own, quite near the first kill. Their clamor drew the dogs back to the scene. But they did nothing this time but look on—there were now 60 hyenas! CONCLUSIONS Pack Function Hunting is undoubtedly the primary func- tion of the free-ranging pack. Wild-dog be- havior is highly specialized and adapted for pack life by dint of the equal and excep- tionally friendly relations between individ- uals, subordination of individual to group activity, discipline during the chase, and close cooperation in killing prey and mutual defense. It may, in fact, be seriously ques- tioned whether a single wild dog could sur- vive for long on its own. As demonstrated by the successful rearing of a litter after the mother died, feeding and protection of the young is another important pack function. The main selective advantages of the pack hunting unit may be summarized as follows: 1. Increased probability of success through cooperation, hence better oppor- tunity to eat regularly at less cost in indi- vidual effort 2. More efficient utilization of food re- sources 3. Less disturbance of prey populations than would result if each animal hunted individually 4. Mutual protection against competitors (spotted hyenas) and possible predators (hyena, leopard [Panthera pardus], and lion ) 5. The provision of food for infants at the den and the adults that remain with them when the pack is hunting, and for juveniles and sick or old adults unable to kill for themselves. Effective Pack Size We have presented evidence, though ad- mittedly tentative, that large packs utilize prey resources more efficiently than small packs, with less waste. Competition from hyenas, where they are numerous, must exert a strong selective pressure in favor of large packs as well as for close cooperation at kills. While the observed tendency for small packs to keep closer together in the chase and at kills would tend to compen- sate somewhat for low numbers, there must be a minimum below which competition from hyenas, and reduced hunting and kill- ing capability, would become a serious handicap. From our observations of both large and small packs, four to six would seem close to the minimum effective unit. We believe that wherever wild dogs are reduced to such small packs, their ability to survive and reproduce may be endan- gered. This is not taking into account the possibility of a differential birth or mor- tality rate that results in a low ratio of fe- males. If it represents a pathological con- dition, this alone could mean that the species is in serious trouble; a prompt in- vestigation of reproduction and neonatal mortality is called for to find out to what extent an abnormally low percentage of fe- males may be responsible for the apparent decline of the species in many parts of Africa. Prey Relations It seems clear that wild dogs are highly selective in the species they prey upon, spe- cializing in East African steppe-savanna on Thomson’s gazelles, and on _ wildebeest 396 THE AFRICAN WILD Doc ° Estes and Goddard = 69 calves during the gnu calving season. Con- sidering their selectivity, their rate of killing, and the observed reactions of herbivores to them, it can only be concluded that wild dogs are by no means so wantonly destruc- tive or disruptive to game as is commonly supposed. Kthme reached the same con- clusion (p. 528). Indeed, until one comes to realize that plains game simply has no place to hide and no sanctuary where predators cannot follow, it is a recurrent surprise to note how short-lived and local- ized are disturbances due to predation. In a prey population as small as that of Thomson’s gazelles in Ngorongoro, if one assumes an average annual recruitment rate of roughly 10 percent, predation at the rate of only one a day obviously would re- duce the population if maintained over a long period. There was, however, no evi- dence that the Thomson’s gazelle popula- tion declined after wild dogs became resi- dent in the Crater; our gazelle censuses in October, 1964, and May, 1965, showed no reduction that could not be accounted for by simple counting errors. Even an actual reduction would have no relevance to the overall situation, as Thomson’s gazelles are the most numerous herbivores in their cen- ters of distribution (the steppe-savanna from central Kenya to north-central Tan- zania ). On the Serengeti Plains, where the gazelle population is estimated at 800,000 and there are probably fewer than 500 wild dogs, predation by this species could have no appreciable effect. Indeed wild dogs are only one of nine predators on the Thom- son’s gazelle (Wright 1960), and not the most important one at that; jackals, which are numerous and specialize in catching new fawns, are probably the main predators. Since wild dogs are nowhere numerous and everywhere apparently specialize on the most abundant small to medium-sized antelopes, it can be argued that more, not fewer, of them are needed. The population explosion of impala in Kruger National Park and many other places where wild dog numbers have declined offers convinc- ing evidence. The high percentage of ter- ritorial males in wild dog kills of Thomson’s gazelles offers a more subtle example of how predation may benefit a prey species: in “probably every gregarious, territorial antelope species, there is always a surplus of fit, adult and young-adult males which cannot reproduce for want of enough suit- able territories, so that the removal of ter- ritorial males by predation is of perhaps major importance in opening up territories for younger and sexually more vigorous males. In our judgment, the wild dog is an in- teresting, valuable predator whose con- tinued survival may be endangered. We feel it should be strictly protected by law in all African states where it occurs, and that it should be actively encouraged, if this is possible, in every park and game re- serve. LITERATURE CITED Bour.iERE, C. F. 1963. Specific feeding habits of African carnivores. African Wildl. 17(1): 21-27. Brown, L. 1965. Africa, a natural history. Ran- dom House, New York. 299pp. BrypEn, H. A. 1936. Wild life in South Africa. George G. Harrap Co. Ltd., London. 282pp. Ha.tTenortH, T. 1963. Klassifikation der Saiuge- tiere: Artiodactyla. Handbuch Zool. Bd. 8. 167pp. Kruux, H. 1966. Clan-system and feeding habits of spotted hyaenas (Crocuta crocuta Erxleben). Nature 209( 5029 ): 1257-1258. Ktume, W. 1965. Freilandstudien ziir Soziologie des Hyadnenhundes. Zeit. Tierpsych. 22(5): 495-541. 1965. Uber die Funktion der rela- Zeit. Tierpsych. LEYHAUSEN, P. tiven Stimmungshierarchie. 22.(4):395-412. MaBERLY, C. T. AstTLEY. 1962. Animals of East Africa. Howard Timmins, Cape Town. 221pp. MACKWORTH-PRAED, C. W., AND C. H. B. GRANT. 1957. Birds of eastern and north eastern Africa. Series I, Vol. I. African handbook 397 70 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 of birds. Longmans, Green and Co., London. 806[ + 40]pp. PercivaL, A. B. 1924. A game ranger’s note- book. Nisbet & Co., London. 374pp. SELous, F. C. 1881. A hunter’s wanderings in Africa. R. Bentley & Son, London. 455pp. STEVENSON-HAMILTON, J. 1947. Wild life in South Africa. Cassell & Co., Ltd., London. 343pp. TuRNER, M., AND M. Watson. 1964. A census of game in Ngorongoro Crater. E. African Wildl. J. 2:165-168. VaucHaAn-Kirpy, F. 1899. The hunting dog. Pp. 602-606. In H. A. Bryden (Editor), Great and small game of Africa. R. Ward Ltd., London. 612pp. Wricut, B. S. 1960. Predation on big game in East Africa. J. Wildl. Mgmt. 24(1):1-15. Received for publication March 21, 1966. 398 November, 1957 GENERAL NOTES 519 HOMING BEHAVIOR OF CHIPMUNKS IN CENTRAL NEW YORK Homing movements ranging from about 150 to 700 yards have been recorded for Tamias by Seton (LIFE HISTORIES OF NORTHERN ANIMALS, vol. 1: 341, 1909), Allen (Bull. N. Y. State Mus., 314: 87, 1938), Burt (Misc. Publ. Mus. Zool. Univ. Mich., 45: 45, 1940), and Hamilton (AMERICAN MAMMALS, p. 283, 1939). While engaged in other studies during the summer of 1952, I had the opportunity of making additional observations on the homing behavior of the eastern chipmunk, Tamias striatus lysieri (Richardson), on the campus of Cornell University at Ithaca, Tompkins County, New York. Live-trapping was conducted from July 26 to August 3 in a tract of approximately 3 acres of hemlock and mixed hardwood forest bordering a small artificiai lake. A maximum of 12 traps was employed. The chipmunks taken were sexed, aged (subadult or adult), marked by clipping patches of fur on various parts of the body, and transported in a cloth bag to one of six release points. The latter were situated in similar continuous habitat or in an area of campus buildings, lawns, shrubbery, and widely spaced trees adjacent to the woodland. An individual was considered as having homed when it was retaken within 115 feet of the original point of capture. Those chipmunks that returned and were recaptured were im- mediately released again in a different direction and usually at a greater distance. First releases averaged 675 feet (310-1,160) and second ones, 1,015 feet (500-1,570). Two animals that returned after second removals were liberated for a third time at distances of 1,130 and 2,180 feet. All distances given are calculated from the station where the animal was originally trapped. Since the mean home range size of chipmunks in this vicinity has been calculated as about .28 acre (Yerger, Jour. Mamm., 34: 448-458, 1953), it is assumed 399 520 JOURNAL OF MAMMALOGY Vol. 38, No. 4 that in most, if not all, instances the removal distances involved were great enough to place the animal in unfamiliar territory beyond the boundaries of its normal range of movements. A total of 18 individuals, consisting of five adult males, four adult females, two subadult males and seven subadult females, were marked and released a total of 29 times through July 30. Animals handled after this date are not included in the treatment of the data, since it is felt that there was insufficient opportunity for them to be retaken following their release. Seven of the chipmunks returned to the vicinity of original capture a total of ten times over distances varying from 430 to 1,200 and averaging 650 feet. In six of the ten returns the animals were retaken in the same trap in which they were initialiy caught. In two instances individuals were retrapped at stations 20 and 40 feet removed from the one where first taken, and in two others the individuals were recovered at a distance of 115 feet from the original site of capture. Two adult males returned from 490 and 540 feet in two and three days, respectively, but were not recovered after second removals to 1,060 and 1,150 feet. Two other maiure males trapped following their release at 310 and 750 feet had moved in a direction other than that of their original capture. An adult female was found in a trap a day after having been released at 775 feet. She returned a second time from 600 feet in two days. Another adult female was retrapped at the original trap station seven days following her release only 430 feet away. A single subadult male was recaptured in his original location the next day after his initial removal to 750 feet and two days after a second liberation at 1,200 feet. He was not retrapped subsequent to a third relocation 2,180 fee: distant. Another young male was captured at a point 350 feet closer to its home area six days after being released 940 feet away. Three subadult females homed successfully. One returned from 580 feet the day after release, another from 650 feet in two days’ time, and the third from 490 feet after an interval of five days. None were retaken foilowing second liberations ranging from 940 to 1,570 feet. Two other subadult females were captured 100 and 120 feet closer to their original capture sites the day after having been released at 460 and 450 feet, respectively. These limited data suggest that homing ability was restricted to rather short distances, only one individual being known to have returned from a point more than 775 feet away. The extent of these movements may be somewhat less than several reported by authors pre- viously mentioned. However, because of the smaller home range size of chipmunks in this area as compared to other habitats in which the animals homed from more distant points, the actual distances moved over strange territory may be fairly comparable. The present results indicate no obvious differences in the proportion of adults and subadults homing nor in the average distance over which individuals in each of these age classes returned. The intervals of one to seven days between releases and recoveries, the relatively short distances involved, and the rather low proportion of returns (38.8 per cent) suggest that the animals may have returned to their home areas through random movements until familiar terrain was encountered. It should be mentioned, however, that the small number of traps employed might have been a factor in the low rate of recovery, since a chipmunk returning to its home region had a lower probability of being recaptured than would have been the case had more traps been present. This might also have tended to increase the apparent time taken to reach the home area following release. On the other hand, the use of a limited number of traps may have been advantageous in that there was less interference by traps with the normal activities and movements of the animals.—JaMes N. Layne, Dept. of Biology, Univ. of Florida, Gainesville. Received December 1, 1956. 400 COMPARATIVE ECHOLOCATION BY FISHING BATS RopDERICK A. SUTHERS ApsTRACT.—The acoustic orientation of two species of fish-catching bats was studied as they negotiated a row of strings or fine wires extending across their flight path. Orientation sounds of Pizonyx vivesi consisted of a steep descending FM sweep lasting about 3 msec. Noctilio leporinus used 8 to 10 msec pulses composed of an initial nearly constant frequency portion followed by a descending frequency modulation. The echolocation of small wires by N. leporinus differed from that of surface fish in that during wire avoidance no nearly constant fre- quency or entirely FM pulses were emitted, nor was the pulse duration markedly shortened as the barrier was approached. There was extensive temporal overlap at the animal’s ear of returning echoes with the emitted cries when the bat was near the barrier—a strong contrast to the apparent careful minimization of such overlap during feeding maneuvers. Noctilio increased its average pulse duration about 2 msec when confronted with a barrier of 0.21 mm, as opposed to 0.51 mm, diameter wires. Pizonyx detected these wires well before pulse-echo overlap began, but at a shorter range than did N. leporinus, suggesting the latter species may have a longer effective range of echolocation. At least two species of Neotropical bats have independently evolved an ability to capture marine or aquatic organisms. A comparison of the acoustic orientation of these animals is of particular interest in view of their convergent feeding habits yet strikingly different orientation sounds. Noctilio leporinus Linnaeus (Noctilionidae) catches fish by occasionally dipping its dispro- portionately large feet into the water as it flies low over the surface. Very small surface disturbances can be echolocated and play an important role in determining the locations of the dips (Suthers, 1965). Fish caught in this way are transferred to the mouth and eaten. Pizonyx vivesi Menegaux (Vesper- tilionidae ) also possesses disproportionately large feet. Much less is known concerning the feeding behavior of this species, though it is reasonable to assume that it uses its feet in a manner similar to N. leporinus (but see Reeder and Norris, 1954). Extensive attempts to induce captive P. vivesi to catch pieces of shrimp from the surface of a large pool were unsuccessful. The fol- lowing comparison is therefore based on the ability of these bats to detect small obstacles. METHODS The experimental animals consisted of two P. vivesi, selected as the best flyers of several collected in the Gulf of California, and one N. leporinus captured in Trinidad. The research was conducted at the William Beebe Memorial Tropical Research Station of the New York Zoological Society in Trinidad. The bats were flown in a 4 X 15 m outdoor cage described elsewhere (Suthers, 1965). The test obstacles consisted of a row of strings or wires 2.5 m long which were hung at 55 cm intervals across the middle of the cage. Four sets of obstacles were used: 2 mm diameter strings, 0.51 mm, 0.21 mm, and 0.10 mm diameter wires, respectively. The bats were forced to pass through this barrier in order to fly the length of the cage. Each 719 401 80 JOURNAL OF MAMMALOGY Vol. 48, No. 1 flight was scored as a hit or a miss according to whether any part of the animal touched the test obstacles. Movement of the larger wires was easily visible following even gentle contact, but lateral illumination of the barrier was necessary in order to score flights through the row of 0.10 mm wires. The wires were occasionally shifted laterally about 20 cm across the width of the cage in order to reduce the possibility that the bats might learn their location. An attempt was made to test each animal on two or more sets of obstacles per night, though this was not always possible. Cases in which the bat was making unusually frequent landings or was particularly reluctant to fly are omitted. Also excluded are flights on which the barrier was approached very near the upper ends of the wires, along either wall of the cage, or at an angle to the row of obstacles which was decidedly smaller than 90°. Experiments with P. vivesi no. 1 were terminated by its sudden death, which oc- curred before the 0.10 mm diameter wire was available. Tests with this size wire were therefore performed with a second healthy Pizonyx. A series of flights through the 0.51 mm and 0.21 mm diameter wires was photographed with a 16 mm sound motion picture camera, while simultaneous two-channel tape re- cordings of the orientation sounds were obtained from microphones placed on opposite sides of the barrier. The position of the flying bat relative to the barrier was calculated by comparing the arrival time of each orientation sound at either microphone and also by matching the image of the bat in each frame of the film with rectified orientation sounds on the optical sound track. Details of these methods and the instrumentation are de- scribed elsewhere (Suthers, 1965). The overall frequency response of the recording sys- tem was approximately uniform between 15 and 100 kc/sec. A total of 45 flights by P. vivesi and N. leporinus was tape recorded and photographed. Sixteen of these were discarded for reasons listed above, or because the bat did not fly on a straight path between the microphones, or because of a poor signal-to-noise ratio on one of the channels. The remaining 29 flights were analyzed and pulse intervals (the silent period from the end of one pulse to the beginning of the next) were plotted against the distance of the bat from the barrier (see Fig. 2). The animal’s position was deter- mined to within an accuracy of about + 10-15 cm at a distance of two meters from the wires and + 5-10 cm in the immediate region of the wires. RESULTS AND CONCLUSIONS Obstacle avoidance scores are given in Table 1. The greater success of P. vivesi in avoiding 0.10 mm wires may reflect its shorter maximum wingspan of 40 cm, compared to 50 cm for N. leporinus. Audio monitoring of the recti- fied orientation sounds emitted by these species during their flights indicated TaBLE 1,—Percent of flights through barrier on which bat missed obstacles spaced at 55 cm intervals. Total number of flights in parentheses. Maximum wingspan of P. vivesi is about 40 cm; that of N. leporinus is about 50 cm. OBSTACLE DIAMETER (MM) Bat 2 0.51 0.21 0.10 Pizonyx vivesi (1) 94% 83% 51% (163) (416) (232) Pizonyx vivesi (2) 71% 37% (151) (74) Noctilio leporinus 91% 76% 60% 20% (207) (203) ella) (55) 402 February 1967 SUTHERS—FISHING BATS Sl FREQUENCY (KG) 0 20 0 60 20 40 TIME (MSEC) Fic. 1.—Sound spectrographs of orientation sounds emitted by Pizonyx vivesi (a) and Noctilio leporinus (b) when approaching wire obstacles. A pair of consecutive pulses, reproduced at two different filter settings of the sound spectrograph, is shown for each species. The narrow band filter setting (top) best indicates the frequency spectrum of the cries, whereas pulse duration and temporal relationships are more accurately shown using a wide band filter (bottom). that approaches to the three larger diameter obstacles were accompanied by increases in the pulse repetition rate, whereas no such increase was noted during approaches to the 0.10 mm wires. This suggests that these latter wires were too small to be detected at an appreciable distance and that tests using them may indicate chance scores. Tape recordings of flights between 0.51 and 0.21 mm diameter wires showed that these two species used distinctly different kinds of orientation sounds in detecting the obstacles (Fig. 1). When approaching the barrier at a dis- tance of about 2 m, P. vivesi emitted ultrasonic pulses with a duration of about 3 msec at a mean repetition rate of 10 to 20 per sec. Each of these was frequency modulated (FM ), sweeping downward from about 45 kc/sec to 20 kc/sec and accompanied by a second harmonic. The slightly lower starting frequency (36 kc/sec) reported by Griffin (1958) may be due to the lower sensitivity to high frequencies of microphones available at that time. At a similar distance from the barrier N. leporinus produced pulses with a duration of about 8 to 10 msec at comparable repetition rates. These sounds, however, were composed of an initial portion at a nearly constant frequency of about 60 kc/sec followed by an FM sweep down to 30 kc/sec. Neither species made any pronounced change in the frequency structure of its pulses as it approached and negotiated 403 82 JOURNAL OF MAMMALOGY Vol. 48, No. 1 PULSE INTERVAL (MSEC) 2 1 0 2 | 0 DISTANCE FROM WIRES (METERS) Fic. 2.—Examples of changes in orientation pulse intervals during flights by fishing bats through a barrier of fine wires spaced at 55 cm intervals across their flight path. Each dot represents one orientation sound: (a) Noctilio leporinus flying between 0.51 mm diameter wires; (b) Pizonyx vivesi flying between 0.51 mm diameter wires; (c) N. leporinus flying between 0.21 mm diameter wires; (d) P. vivesi flying between 0.21 mm diameter wires. On flights a, b, and d, the bat did not touch the wires. On the flight shown in c the wires were hit by the bat. Vertical dashed line indicates position of the wires. the barrier. The pulse repetition rate was increased, however, to about 30 or 35 per sec. The use of a single pulse type by N. leporinus contrasts with its echolocation during normal cruising and feeding when constant frequency and entirely FM pulses are also employed (Suthers, 1965). Fig. 2 gives examples of alterations in pulse intervals during one flight by each species through a barrier of 0.51 mm and of 0.21 mm diameter wires. The possible significance of the tendency to alternate long and short pulse intervals during the approach to the barrier’is not known. It was not possible to reliably distinguish hits from misses on the basis of these graphs. The minimum average distance of detection was estimated by calculating the point at which the bat began to shorten the pulse intervals. Pizonyx vivesi and N. leporinus must have detected the 0.51 mm wires at an average distance from the barrier of at least 110 and 150 cm, respectively, and the 0.21 mm 404 February 1967 SUTHERS—FISHING BATS 83 | | ve) 7 ZO~ |e ow ae =~ x = = 02 =o, ‘ 100 PULSE INTERVAL (MSEC) PULSE DURATION (MSEC) 80 60 40 O~ ~—o~ ~o- 0, im | Pia -9 ~ Pm mon Om 4220-07 20 2 I 0 DISTANCE FROM WIRES (METERS) Fic. 3.—Mean pulse intervals (solid line) and mean pulse duration (broken line) of Noctilio leporinus (a) and Pizonyx vivesi (b) during approaches to the 0.51 mm diameter wires spaced across the flight path at 55 cm intervals. The bat is flying from left to right. Vertical dashed line indicates the position of the wires. Arrows indicate estimated minimum mean distance of detection as judged by progressive shortening of the pulse intervals. Dotted diagonal line shows the distance at which pulse-echo overlap will first occur for any given pulse duration. Echoes from the wires of pulses whose mean duration lies above this line will overlap with the emitted pulse by an average amount equal to their vertical distance above the line. Each point represents the mean interval or duration of pulses emitted in the adjacent + 10 cm. Intervals for N. leporinus are averages of five flights; P. vivcsi intervals, of seven flights. All pulse durations are averages of three flights. 405 84 JOURNAL OF MAMMALOGY Vol. 48, No. 1 100 80 60 40 20 100 PULSE INTERVAL (MSEC) PULSE DURATION (MSEC) 80 60 40 2 1 0 DISTANCE FROM WIRES (METERS) Fic. 4.—Mean pulse intervals (solid line) and mean pulse duration (broken line) of Noctilio leporinus (a) and Pizonyx vivesi (b) during approaches to the 0.21 mm diameter wires spaced across the flight path at 55 cm intervals. For explanation see legend of Fig. 3. Possible alternate interpretations of the point at which a progressive decrease in pulse intervals first appears are indicated by small arrows. The more conservative estimates denoted by the large arrows have been used in the text. Pulse durations and intervals of N. leporinus are averages of 10 flights; those of P. vivesi are averages of seven flights. 406 February 1967 SUTHERS—FISHING BATS 85 wires at an average of at least 70 and 130 cm, respectively (Figs. 3 and 4). Pulse durations did not markedly shorten as the barrier was approached. Thus at close ranges the echoes returning from the wires must have overlapped extensively with the emitted pulse. In the case of N. leporinus this overlap may have begun on the average when the bat was still 130 and 170 cm from the 0.51 and 0.21 mm wires, respectively (Figs. 3 and 4). The data do not exclude the possibility that the start of pulse-echo overlap and the start of a progressive reduction in the pulse intervals by N. leporinus may occur simultaneously or be closely synchronized. The pulses of P. vivesi must have overlapped with their echoes during the last 40 and 50 cm of the approach to the 0.5) and 0.21 mm wires, respectively (Figs. 3 and 4). It seems clear that P. vivesi bezan to decrease its pulse intervals well before the first pulse-echo overlap occurred. Noctilio leporinus regularly emitted longer pulses when approaching the 0.21 mm wires than when approaching the 0.51 mm wires. The significance of this difference is not known, although it is possible that the earlier initiation of pulse-echo overlap, or the increased duration of overlap at a given dis- tance, when longer pulses are used, in some way facilitated detection of the finer wires. If this is true, however, why is overlap minimized with such apparent care during the detection of small cubes of fish muscle tissue pro- jecting above the water surface (see below)? Since the difference in pulse duration as a function of wire diameter was already present when the bat was two meters from the barrier, either leporinus must have determined some- thing about the wire diameter at a distance of more than two meters, or it must have remembered what kind of wires it had to detect and adopted a suitable pulse duration prior to their detection. Details of the echolocation of P. vivesi during feeding are not known. Pulse- echo overlap during wire avoidance by N. leporinus, however, contrasts strongly with its apparent careful avoidance during catches of stationary 1 cm? cubes of fish muscle tissue projecting above the surface of the water. Pulse lengths under these conditions were progressively shortened as if to avoid pulse-echo overlap until the bat was 30 cm or less from the food (Suthers, 1965). Thus in the case of N. leporinus, at least, information concerning the position and nature of small wire obstacles is probably received in the presence of overlap, whereas most of this information regarding potential food must be obtained without such overlap. It has yet to be determined whether or not pulse-echo overlap is actually utilized by the bat. It has been suggested (Pye, 1960; Kay, 1961) that possible nonlinearities in the ear may allow bats to utilize beat notes arising from pulse-echo overlap as a means of determining distance. Three species of chilonycterine bats have subsequently been found to maintain an overlap during the pursuit and catch- ing of Drosophila (Novick, 1963, 1965; Novick and Vaisnys, 1964). Myotis lucifugus (Cahlander et al., 1964) and N. leporinus, on the other hand, appear to minimize overlap when catching tossed mealworms or fish, respectively. 407 86 JOURNAL OF MAMMALOGY Vol. 48, No. 1 Should pulse-echo overlap be utilized by N.\leporinus in determining its dis- tance from the wires, then some basically different method, such as the temporal delay of the returning echo (Hartridge, 1945), must be employed in determining the range of potential food. Since the constant frequency portion of the Doppler-shifted echo would at first overlap with the FM portion of the call, and later with part of both the constant frequency and FM portions of the call, any resulting beat note would have a complexly varying frequency structure from which it would be difficult for the bat to determine its distance from the barrier. One would like to know if there is a significant difference in the range of echolocation for these fishing bats. Noctilio leporinus emits very loud pulses with a peak-to-peak sound pressure of up to 60 dynes/cm? at a distance of 50 cm from the mouth (Griffin and Novick, 1955). The intensity of sounds emitted by P. vivesi has not been measured, although the shorter range at which they can be detected on an ultrasonic receiver suggests they are less intense than those of Noctilio. M. lucifugus, a vespertilionid closely related to Pizonyx, can detect 0.46 mm diameter wires at 120 cm and 0.18 mm wires at 90 cm (Grinnell and Griffin, 1958), thus comparing favorably with fishing bats in this respect. Peak-to-peak sound pressures of this species have been measured at 12 dynes/cm? at 50 cm (Griffin, 1950). Sound intensity of the emitted pulse, however, is but one of a number of physical and physiological factors which must play important roles in determining the range of such a system for acoustic orientation. ACKNOWLEDGMENTS I wish to thank Prof. Donald R. Griffin, Drs. H. Markl, N. Suga, and D. Dunning for helpful criticism and assistance. Drs. R. E. Carpenter, G. W. Cox, and A. Starrett gave valuable assistance in obtaining live P. vivesi. Appreciation is also expressed to the San Diego Society of Natural History for use of the Vermillion Sea Station at Bahia de los Angeles, Baja California, and to the New York Zoological Society for the use of the William Beebe Memorial Tropical Research Station in Trinidad. The coopera- tion of the Mexican, Trinidadian, and United States governments in the transit of bats is gratefully acknowledged. This work was supported by grants from N.I.H., The Society of the Sigma Xi Research Fund, and the Milton Fund of Harvard University. LITERATURE CITED GnrirFiIn, D. R. 1950. Measurements of the ultrasonic cries of bats. J. Acoust. Soc. Amer., 22: 247-255. 1958. Listening in the dark. Yale Univ. Press, New Haven, 413 pp. GriFFIN, D. R., anp A. Novick. 1955. Acoustic orientation of neotropical bats. J. Exp. Zool., 130: 251-300. GRINNELL, A. D., AND D. R. GrirFin. 1958. The sensitivity of echolocation in bats. Biol. Bull., 114: 10-22. Hartrivce, H. 1945. Acoustic control in the flight of bats. Nature, 156: 490-494. Kay, L. 1961. Perception of distance in animal echolocation. Nature, 190: 361-362. Novick, A. 1963. Pulse duration in the echolocation of insects by the bat, Pteronotus. Ergebnisse Biol., 26: 21-26. 408 February 1967 SUTHERS—FISHING BATS 87 1965. Echolocation of flying insects by the bat, Chilonycteris psilotis. Biol. Bull., 128: 297-314. Novick, A., AND J. R. Vaisnys. 1964. Echolocation of flying insects by the bat, Chilonycteris parnelli. Biol. Bull., 127: 478-488. Pye, J. D. 1960. IYM Ul saiONbs a120-| "9 $O UOI}DjNWNDD0 UO pasng alam saHuds aWOH “Z| Ajnf UO YyJIG S}I JayJO spoisad sMolsDA JO} 6ZZ a]DW Bunod jo saBuns awoy ‘py “B14 Pe aS eS a ax 3 qd dWYMS N3dO NV1dN GagdOOM ee es ee cr ee fe as ioe tL190 - 1 190 1334 0021 lz 5 nv O€ 1d3S - 91 1d3S q Pe Al t as seat fame fem MAA mane a "aad £2 1Nf 90 ur Stn ir le ed i ENS f ‘com oa Ye : 439 BEHAVIOR OF YOUNG SNOWSHOE Hares + Rongstad and Tester conclude that young hares remain together for only 1 to 4 days and thereafter scatter in the area around the place of birth. On the day after release from the pen (day 8), all young were located with a portable receiver. Each was in a separate hiding place, and was separated from the others by as much as 60 feet. All were caught without a chase. On July 22, 3 days after release, the young were spaced about the same as on July 20 and were again caught without a chase. However, two ran after being released. On July 25 the young were caught, and batteries on the trans- mitters were changed. At this time, young were separated by up to 100 feet, and only one was caught without a chase. One had to be chased for at least 500 feet before it could be captured. On August 2, the trans- mitter on one animal stopped; the other three were captured (one without a chase ) for a battery change. The daytime resting places of the three were still farther apart than on July 25. A weasel killed one of these young on the night of August 7-8; the other two lived through the winter. Even though these young hares were carrying radio transmitters and could be captured without a chase, they were dif- ficult to find. They remained motionless and were usually in small forms, concealed by vegetation. Based on locations obtained with the tracking system, home ranges of the young of female 225 were between 1.6 and 2.4 acres during their second week of life (Table 1). Home ranges increased slightly during the third, fourth, and fifth weeks and showed major increases in the sixth and seventh weeks. After 8 weeks, home-range sizes were about the same as for adults. We do not know how the long nursing period affected home ranges. However, one young hare, estimated to be 25 days old when trapped, had a home range of 5.8 345 Figs.5: 225 for their 2nd (A) and 3rd week of life (B). squares indicate the number of times a particular animal was Upper left number is for male 227, Combined home ranges of the four young of female Numbers in located in that square. upper right for female 228, lower left for male 229, and lower right for female 230. The stars indicate the same ref- erence point for both home ranges. acres for 10 days after capture. Another, estimated to be 60 days old when trapped, had a home range of 8.7 acres for 10 days after release, and 15.8 acres for the next 7 days. These home-range estimates are sim- ilar to those for the pen-released young of female 225. For young male 229, changes in home- range size, shape, and intensity of use are shown in Fig. 4. The home ranges for its littermate (female 228), which lived through the winter, were approximately the same size (Table 1), and both animals lived in the same general area until November 14; at that time, hare 228 moved to a brushy lowland about 1,500 feet east of the area it had previously used. The January home range, therefore, did not overlap its pre- vious home ranges. The entire area used by the four young during their 2nd and 3rd weeks of life was 2.8 acres and 4.8 acres, respectively (Fig. 5A, B). Even at this early age, the young seemed to have spaced themselves. When we looked at only the five most intensively used 0.l-acre squares for each young, we found that the 0.5 acre used by No. 229 and the 0.5 acre used by No. 230 were not used 440 346 intensively by any other animal and that No. 227 and No. 228 had only two squares in common. Our data indicate that the young as- sembled each night about 5 to 10 minutes before the female returned, even on August 26 when, as described above, the female was 20 minutes earlier than on any previous night. The same mechanism was probably triggering the timing of the female and her young. The gathering place did not appear to be rigidly fixed, apparently varying by 30 to 50 feet between nights, but this was difficult to determine precisely because of limitations in the tracking system. LITERATURE CITED Cocuran, W. W., D. W. Warner, J. R. TESTER, AND V. B. KuEcHLE. 1965. Automatic radio- tracking system for monitoring animal move- ments. BioScience 15(2):98—100. 44] Journal of Wildlife Management, Vol. 35, No. 2, April 1971 HEEZEN, K. L., AnD J. R. TESTER. 1967. Evalua- tion of radio-tracking by triangulation with special reference to deer movements. J. Wildl. Memt. 31(1):124-141. KeiTH, L. B., E. C. MEsLow, AND O. J. RoNGSTAD. 1968. Techniques for snowshoe hare popula- tion studies. J. Wildl. Mgmt. 32(4):801-812. Mecu, L, D., V. B. KUECHLE, D. W. WARNER, AND J. R. Tester. 1965. A collar for attaching radio transmitters to rabbits, hares, and rac- coons. J. Wildl. Mgmt. 29(4):898-902. RoncstTapD, O. J., AND J. R. TEsTER. 1969. Move- ments and habitat use of white-tailed deer in Minnesota. J. Wildl. Mgmt. 33(2):366-379. SEVERAID, J. H. 1942. The snowshoe hare; its life history and artificial propagation. Maine Dept. Inland Fisheries and Game. 95pp. VENGE, O. 1963. The influence of nursing behaviour and milk production on early growth in rabbits. Animal Behaviour 11(4):500-506. ZARROW, M. X., V. H. DENENBERG, AND C, O. ANDERSON. 1965. Rabbit: frequency of suckling in the pup. Science 150(3705):1835 -1836. Received for publication September 25, 1970. er owned VA sat lees 2 1 ya: ~ Mehr + h" rp jtesct } 7 hy bid t 154¢. tit rewat it ih Loerie pihiaty irtesh J VveiW by. pelay ated SECTION 5—PALEONTOLOGY AND EVOLUTION If there be one unifying principle that pervades all of biology, it is that of evolution. Not only is this evident in consideration of the papers here repro- duced (which range from one that deals in part with intrapopulational varia- tion up to those concerned with higher taxonomic categories), but it also is evident in the contents of virtually all other papers chosen for inclusion in this anthology. The few selections in this section, then, provide but a glance at some aspects of mammalian evolution. The short paper by Reed nicely illustrates some problems that increases in knowledge have generated in our own part of the evolutionary tree. Linked inseparably with the evolutionary process is the fossil record, which is un- usually good for some groups of mammals and provides much of the raw data for phylogenetic considerations. For papers relating to paleontology, we have chosen one (Wilson) that alludes to the importance of sound geographic and stratigraphic data and that ties in with the historic record, one (Radinsky ) that deals with evolution and early radiation of perissodactyls, and two on rodents, one a paper by Zakrzewski revising the muskrat tribe, and the other a modern treatment of the major groups of the extremely complex order Ro- dentia by Wood (see also Wood, 1959). For a recent analysis of one major group of rodents that includes good dis- cussions of relationships, see Rowlands and Weir (1974). An excellent short overview of rodent evolution was written by Wilson (1972). Two areas of recent interest that should be mentioned are the use of observable wear facets in attempts to understand function of teeth and cusps (for example, Crompton and Sita-Lumsden, 1970), and the elucidation of plate tectonics and moving continental land masses as significant factors in evolution and zoogeography (for example, see McKenna, 1973). The study by Guthrie compares evolutionary change in molar teeth and relates this to variability in different measurements, using both fossil and Recent species of Microtus, and thus stresses the on-going evolutionary process. The elephants are represented by a good fossil record, and show major changes in dentition that led to better grinders, just as in the microtines studied by Guthrie. These changes and their functions in elephants were analyzed by Maglio (1973). Variability within populations of mammals has been sum- marized by Yablokov (1974). The paper by Jansky is interesting because it provides an excellent example of evolutionary trends in features other than those directly related to “hard anatomy.” Nadler et al. studied the evolution of one species of ground squirrel in a relatively small area by examining chromosomes. The study by Smith ef al. demonstrated striking differences between survival of wild- and laboratory- reared mice in a wild environment, even though it failed to reveal any effect of color on natural selection, which was the main hypothesis in initiating the study. Some earlier and later studies have revealed selective effects of color in small mammals (for example, Kaufman, 1974). Species have not evolved in isolation but in ecosystems. The paper by Heithaus et al. examines the coevolution of certain tropical bats and plants. 443 The literature of mammalian evolutionary and paleontological studies is widely scattered. Aside from the journals and bibliographic sources mentioned in the Introduction, the interested student should consult EvoLturion, the JOURNAL OF PALEONTOLOGY, and the recently initiated PALEoBioLocy. He should also be aware of the Bibliography of Fossil Vertebrates, 1969-1972, compiled by Gregory et al., 1973 (as well as earlier volumes in the same series ) and the News Bulletin of the Society of Vertebrate Paleontology. Romer’s textbook, Vertebrate Paleontology (1966) and Simpson’s (1945) The Principles of Classification and a Classification of Mammals are especially recommended as sources of considerable information on the fossil history and evolution of mammals, and we would be remiss not to mention also Zittel’s (1891-93) classic Handbuch der Palaeontologie (volume 4, Mammalia). Two substantial longer papers on systematics and evolution of special groups are Dawson's (1958) review of Tertiary leporids, and Black’s (1963) report on the Tertiary sciurids of North America. Extensive paleofaunal studies of note are many: those by Hibbard (1950) on the Rexroad Formation from Kansas and by Wilson (1960) on Miocene mammals from northeastern Colorado serve as excellent examples. South African Journal of Science Suid-Afrikaanse Tydskrif vir Wetenskap The Association, as a body, is not responsible for the statements and opinions advanced in its publications. Die Vereniging is nie, as ‘n liggaam, verantwoordelik vir die verklarings en opinies wat in sy tydskrifte voorkom nie. Vol./Deel 63 JANUARY 1967 JANUARIE No. 1 THE GENERIC ALLOCATION OF THE HOMINID SPECIES HABILIS AS A PROBLEM IN SYSTEMATICS CHARLES A. REED HE recent controversial discussion, in as he emphasizes in his own thinking about Current Anthropology (Oct. 1965) and the material, the greater or lesser degree of elsewhere, concerning the correct generic morphological likenesses between two popu- placement of the Lower Pleistocene hominid lations which have essentially reached, at the species /iabilis (Leakey, Tobias, and Napier, generic or specific levels, a considerable 1964), depends for its soluuon upon which similarity. Obviously, the individuals of one of two kinds of philosophy of systematics habilis are anatomically more similar to is followed. None of the participants in the individuals of Ausrralopithecus africanus discussion have emphasized this particular that they are to ourselves as Homo sapiens, aspect of the issues, but an understanding of or even to individuals of the mid-Pleistocene these concepts is basic to both argument and taxon H. erecrus. Robinson (1965a, b) and solution. separately Howell (1965), seeing clearly this If one is impressed with the phylogenetic essenual anatomical similarity between approach to the study of fossils, stressing africanus and habilis, wish to emphasize the implications of those evoluuonary inno- what to them is a clear closeness of biological vations found in them which place a parti- relationship by placing the two populations cular group at the beginning of a new together in the same genus, Australopithecus evolutionary line, leading in time to new in this instance.* adaptve possibilities, then the classification The issues involved have roots deep in the will be vertical (‘classification by clade’). history of post-Darwinian systematics, parti- Utilizing this approach to zoological syste- cularly as practised by palaeoniologists. matics the invesugator will emphasize the Simpson (1961) has summarized the problems importance of the new evolutionary direction with a suggestion for a solution which (the new adaptive plateau being approached), attempts (although in my opinion not by placing his fossils in the taxon with the : * The mentioning of two genera, but only two, as coinprising the advanced forms derived from them. Leakey, known Quaternary hominids is done on the basis of the general Tobias. and Napier did exactly this when usage of the authors involved in the controversy presently being ; : ope considered, and with the view that Paranthropus 1s probably best they placed the population habilis, from considered as a sub-genus of Australopithecus. We must not j 1 ; forget, however, that Mayr (1950) advocated that all Quaternary Bed I of Olduvai Gorge, Tanzania, In the hominids be included in Homo, a practice followed only inter- genus Homo (Fig. 1). mittently thereafter but espoused in at least two recent textbooks . (Brace and Montagu, 1965; Buettner-Janusch, 1966). There 1s The alternate approach to systematics 1S also another possible point of view, the one that Aabilis be included “classification by grade,” wherein the investi- within Homo erectus, probably as a subspecies, although Tobias 4 5 (1965b) has indicated that on the basis of present evidence this 1s gator emphasizes in his taxonomic system, a conclusion with which he could not agree. South African Journal of Science 3 January, 1967 445 Pleistocene Lower Phocene Fig. 1: Phylogeny and classification of the Family Hominidae, as presently understood (after Tobias, 1965a). The dotted line represents the boundary in time and between the taxa Homo and Australopithecus as conceived on the basis of classification by clade; the dashed line represents the same concepts on the basis of classification by grade. successfully) to combine the two approaches. An earlier paper by myself (Reed 1960), as based on publications listed in its biblio- graphy, states these particular issues in a shorter article and also points out the logical consequences of accepting either system, that ‘“‘by clades” or the contrasting one, “by grades.” Neither system is necessarily correct, nor either wrong; they simply are based on two different, and in my opinion mutually exclusive, approaches to the systematic organization of biological populations in a time-continuum. For this reason, systematics remains an art and is not a science, depending upon the opinion of trained investigators for decisions which eventually are or are not followed by larger numbers of people who are interested in the fossils and the phylogeny, but have neither the time nor training to study the materials in detail. Januarie 1967 446 Our problems with the systematics emerg: irrevocably from the pattern of a continuous flow of genes, generation by generation, and from the occasional divisions of a popu- lation’s gene pool into separate evolutionary streams. The vertical type of classification based on clades is possible only if a population has proved its survival value by becoming the ancestral type of a new lineage, and if we have found a good record of these happen- ings. Thus if the population habilis had become extinct during the period of the formation of Bed I at Olduvai Gorge, its evolutionary potential would be unrecog- nizable and its remains would most certainly be classified with Australopithecus by what- ever subsequent intelligent being was doing the paleontology. The Homo-ness of habilis lies in those characters which we can recog- nize as being important in initiating the lineage Homo only because we have a record of that lineage. Until, however, we had as complete a record of that lineage as we finally now have, systematics by clade was not possible. A bit of an analogy, involving non- hominid lineages with which we are not personally involved, may help to clarify the principles. Thus the phylogenies of two super-families, those of the horses (Equoidea) and of the tapirs (Tapiroidea), diverged early in the Eocene. The first-known indi- vidual fossils of each of these two super- families are extremely similar, but each—to the eye of the expert—indicates its affinities to its known descendants by what might appear to be, but is not, a trifle of dental pattern (Radinsky, 1963). Where the fossil record is as complete as with these perisso- dactyls, the solution of the systematic problems has typically been to include in different clades (families or super-families) different populations which on the basis of similarity of anatomical form would be grouped at the grade level as closely related genera or as species in the same genus. If, at this Eocene level of evolution, one of these ancestral groups. such as Hyracotherium (ancestral to all later “horses” sensu Jato), Suid-Afrikaanse Tydskrif vir Wetenskap had become extinct, no palaeontologisi would be capable of recognizing its potential “horse-ness’ and Hyracotherium would today be classified as a primitive tapir. Conversely, if Homogalax, the earliest of the tapiroid line, had become extinct without issue, undoubtedly it would today be classi- fied as an Eocene equid. In general, as the gaps in the fossil record of any lineage have been filled, the tendency has been, often without any realization of the philosophy of the systematics involved, to shift from a horizontal (grade) type of classification to the vertical (clade) type, and the recent flurry of published opinions as to the formal position of the species habilis illustrated a repetition of this historical pattern. Tobias (196Sc) has stated that there is general agreement as to the meaning of the morphological data and the validity of the evolutionary position of the fossils included in the population habilis from Bed I at Olduvai Gorge; if precedent has any value as a guide, we may safely assume that habilis will remain in Homo. In general, the Primates have been classi- fied on the principle of grades, typical of groups with an incomplete fossil record and thus lacking well-defined lineages. As more fossils are found and the phyletic pattern becomes clearer, various parts of the sub- order (grade) Prosimi will become con- tinuous with at least two lineages (platyrrhine and catarrhine) of the suborder (grade) Anthropoidea, and slowly the present pattern of the systematics will change. Exactly this sort of change, to the surprise of some, is what is occurring in the Homini- dae, due to the filling of the gaps priorly existing between the groups called Australo- pithecinae and Homininae. We should realize also that, as now defined, the names applied to extinct populations of Homo remain as grade concepts, as has already been stated clearly by Tobias and von Koenigswald (1964). Thus, if and when human fossils are found to fill the near-void now existing between the latest erectus and the earliest acknowledged neandertals, the South African Journal of Science 447 whole present taxonomic scheme will neces- sarily be changed from the horizontal to the vertical. Perhaps that agonizing re- appraisal will be easier then—as indeed I hope it will be now at the /abilis level— if we realize that it is inevitable. REFERENCES CITED Brace, C. L. and M. F. ASHLEY MONTAGU (1965): Man's evolution: An introduction to physical anthropology. New York, The Macmillan Com- pany. BUETTNER-JANUSCH, JOHN (1966): Origins of Man: Physical Anthropology. John Wiley and Sons, Inc. New York. HoweE__, F. Criark (1965): Early man. New York: Life Nature Library, Time Incorporated. Leakey, L. S. B., Tosias, P. V. and Napier, J. R. (1964): A new species of genus Homo from Olduvai Gorge. Nature 202:7-9. (Reprinted 1965 in Current Anthropology, 6:424-27). Mayr, Ernst (1950): Taxonomic categories in fossil hominids. Cold Spring Harbor Symposia in Quanti- tative Biology 15:109-18. RADINSKY, LEONARD (1963): Origin and evolution of North American Tapiroidea. Peabody Museum of Natural History, Yale University, Bulletin 17, 1-106. REED, CHARLES A. (1960): Polyphyletic or mono- phyletic ancestry of mammals, or: What 1s a class? Evolution 14, 314-22. Rosinson, J. T. (1965a): Homo ‘habilis’ and the australopithecines. Nature 205, 121-24. (1965b): Comment on “New discoveries in Tanganyika: Their bearing on hominid evolution,” by Phillip V. Tobias. Current Anthropology 6, 403-6. SIMPSON, GEORGE GAYLORD (1961): Principles of animal taxonomy. New York: Columbia University Press. TosIAS, PHILLIP V. (1965a): Early man in East Africa. Science, 1949, 22-33. (1965b): Homo habilis. Science 149, 918. (1965c): New discoveries in Tanganyika: Their bearing on hominid evolution. Current Anthropology 6, 391-99. Tosias, P. V. and VON KOENIGSWALD, G. H. R. (1964): A comparison between the Olduvai hominines and those of Java and some implications for hominid phylogeny. Nature 204, 515-18. (Reprinted 1965 in Current Anthropology 6, 427-31). DEPARTMENTS OF ANTHROPOLOGY AND BIOLOGICAL SCIENCES, UNIVERSITY OF ILLINOIS AT CHICAGO CIRCLE, CHICAGO, ILLINOIS, U.S.A. January, 1967 FOSSIL ONDATRINI FROM WESTERN NORTH AMERICA RicHARD J. ZAKRZEWSKI ApstTrAct.—The cranium of Pliopotamys minor (Wilson) from the Hagerman local fauna is described. The cranial elements show a mosaic of shapes found in other distantly related arvicoline genera. The size of the cranium and the ratio of certain cranial measurements most closely approximate the extant genera Neo- fiber and Arvicola, which suggests a similar structural grade for the three genera. A partial cranium of a relatively advanced ondatrine recovered from deposits equiv- alent to those which contain the late Pliocene Benson local fauna is reported from Arizona. The stage of evolution of this animal is similar to species previously de- scribed from the early Pleistocene. These relationships suggest an early radiation of Ondatrini in the American southwest. Two partial lower jaws of a primitive on- datrine are reported from the San Joaquin formation of California. The nature of the specimens precludes generic assignment. Isolated teeth and mandibles of arvicolines are common in deposits of late Cenozoic age. Remains of complete crania, however, are rare. Only one cra- nium of an extinct genus of arvicoline, Cosomys, has been described from North America (Wilson, 1932); therefore, the find of an almost complete cranium of Pliopotamys minor (Wilson, 1933) from the Hagerman local fauna, late Pliocene of Idaho, is significant. Additionally the partial cranium of an ondatrine from Arizona, found in deposits equivalent to those that contain the Benson local fauna (late Pliocene), and two partial lower jaws of a prim- itive ondatrine from the San Joaquin formation of California are discussed. Specimens of Ondatrini from these latter two sites have not been reported. MATERIAL The cranium of Pliopotamys minor (Idaho State University Museum, no. 17123) was found by John A. White and myself in May 1969, at the United States Geological Survey Cenozoic locality 20765 (for complete locality data see Hibbard, 1959). The specimen is slightly compressed dorsoventrally. The left zygomatic arch, auditory bullae, and all the teeth except the upper right first molar are missing. I recently (1969) reviewed the systematic position of Pliopotamys and considered it to be ancestral to Ondatra. To find out more about the relationships of Pliopotamys I have compared the cranium of ISUM 17123 with crania from Recent species of Ondatra, Neo- fiber, Microtus, Neotoma, and Arvicola. The specimen from Arizona (Frick Collection, American Museum of Natural History, no. 24649) is a partial cranium with a portion of the frontal, palatine, maxillaries, and all the molars except the upper left third molar present. The fossil was found 3.5 miles south of Benson, Arizona. I compared it with the cranium from the Hagerman local fauna and with isolated teeth of Pliopotamys meadensis Hibbard, 1938, and Ondatra idahoensis Wilson, 1933. The specimens from California (University of California, Museum of Paleontology, nos. 32952 and 57958) are two partial mandibles with the first two molars present in both; however, the anterior loop on the lower first molar in each of the specimens is broken off. The specimens were found in the San Joaquin formation (UCMP locality V3520). I 284 May 1974 ZAKRZEWSKI—FOSSIL ONDATRINI 285 compared these mandibles with mandibles of Pliopotamys minor and Cosomys primus from the Hagerman local fauna, and with the holotype of C. primus from the Coso Moun- tain local fauna of California. The tribe Ondatrini, as defined by Kretzoi (1969), is used here for convenience in discussion. CRANIUM FROM HAGERMAN The size of the cranium in Pliopotamys minor is approximately equal to that of the woodrat, Neotoma lepida Thomas, 1893. The cranium of Plio- potamys, however, is typically arvicoline in structure. Arvicoline affinities are evident especially in the shape of the zygomatic plate, which expands ventrally and laterally rather than anteriad as in Neotoma, and in the con- figuration of the postorbital processes that extend at right angles to each frontal bone. Viewed dorsally (Fig. 1B), the nasals of Pliopotamys minor are short, ex- pand anteriorly, and flare slightly lateroventrally; they most closely resemble those of Ondatra. The frontals of Pliopotamys minor end anteriorly in a W-shaped suture pattern; a pattern that resembles those in Ondatra and Neofiber. Posteriorly the shape of the frontal most closely resembles that of Arvicola in that the suture is concave anteriorly. The frontals of Pliopotamys possess low inter- orbital crests, like those in the other arvicoline genera I examined. In P. minor the crests abut just posterior to the least interorbital constriction. Anterior to this constriction the crests separate and continue forward until they end at the juncture of the premaxillaries and nasals. Just anterior to the inter- orbital area a small fossa is present between the crests making them appear well developed. Even though the development of the crests can vary with the ontogenetic age of the individual, I found a similar configuration and development of the fossa only in Ondatra and the ondatrine from Arizona. Posteriorly the crests separate and follow the lateral sutures of the parietals as temporal ridges to the end of the cranium. I found this configuration in Arvicola as well, but the interorbital crests in P. minor begin to separate more anteriorly. The parietals of Pliopotamys minor resemble those of Neotoma cinerea. The interparietal is shaped like that in Microtus ochrogaster. In lateral view (Fig. 1A), even though some dorsoventral compression has taken place, the profile of the cranium in Pliopotamys was lower than in ex- tant arvicolines, being more like that in Neotoma. The portion of the maxillary in which the alveoli are situated is separated from the rest of the cranium by the optic and sphenopalatine foramina. This portion of the maxillary in Pliopotamys can be considered shallow or narrow when compared to extant arvicolines. A similar condition exists in Neotoma, this reflects the fact that in both Pliopotamys and Neotoma the molars are mesodont and have well-developed roots. 449 286 JOURNAL OF MAMMALOGY Vol. 55, No. 2 il / WW 5mm \\ HU : | Me . dh \\ I, B ( ay Sh ree) I'l D5 f Shas SS Ml \ \? | \ YO I a \ \\ WAN ; SI fl ( \ A\\ ~ X ill nN ", ee UX I, Ay | NA vn, f- \ Fic. 1.—Cranium of Pliopotamys minor (Wilson); A, lateral view; B, dorsal view; C, ventral view. In ventral view (Fig. 1C) the incisive foramina of Pliopotamys minor are as long as they are in Neotoma lepida. However, the length of incisive fo- ramina varies with the ontogenetic age of the individual as has been pointed out by Quay (1954) for extant arvicolines and by Hibbard and Zakrzewski (1967) and Zakrzewski (1969) for extinct arvicolines. 450 May 1974 ZAKRZEWSKI—FOSSIL ONDATRINI 287 TABLE 1.—Measurements (in millimeters) of the cranium (ISUM 17123) of Pliopotamys minor Parameter Measurements Parameter Measurements Length of alveolar molar row 10.0 Diastema length iy, Greatest length of skull 38.5 Length of palatal bridge 9.1 Basal length 36.6 Breadth of braincase 14.6 Basilar length 34.0 Zygomatic breadth leet ete Palatal length 21.8 Breadth of rostrum Tee Palitar length 19.5 Least interorbital breadth 62% * = estimate + = width from midline to edge of right zygomatic arch multiplied by two The lateral palatal grooves in Pliopotamys are moderately deep and the maxillary walls which form the outermost portion are vertical. These con- figurations most closely resemble those found in Ondatra. These grooves ex- tend from the posterior end of the palate forward into the incisive foramina. The median ridge is narrow, elevated throughout its entire length, and widens posteriorly. These configurations were observed in maxillaries of other Pliopotamys I examined earlier (Zakrzewski, 1969). The median ridge of Neofiber resembles that of P. minor in that it is elevated throughout its entire length. However, in Pliopotamys the ridge is solid throughout its length, whereas in Neofiber there is a slight groove running down the central portion of the median ridge to a position just posterior to the first molars, where the central part of the ridge becomes elevated into a narrower ridge. Because the tympanic bullae are missing from the cranium the pterotic bones are exposed. They are globular in shape. Although part of the pterotic bone toward the midline of the skull is damaged, it does not appear as flattened and fanned out as it is in Ondatra. The overall shape of the pterotic in Plio- potamys most closely resembles that of Neofiber. Due to postdepositional damage the other portions of the cranium cannot be accurately described. Measurements of 12 parameters of the skull were taken from the cranium of Pliopotamys using the definitions of Hershkovitz (1962), and are listed in Table 1. These same measurements were taken from small samples of extant Ondatra zibethica, Neofiber alleni, Arvicola terrestris, Microtus ochrogaster, and Neotoma cinerea. The relationship of these measurements is shown ( Fig. 2) by means of a ratio diagram (Simpson et al., 1960). Apparently Pliopotamys possessed characteristics that exist today in dis- tantly related arvicoline groups, as well as some that exist in the unrelated Neotoma. However, Pliopotamys has more characters in common with the extant amphibious arvicolines, especially Ondatra. In the measured param- eters Pliopotamys tends to parallel the medium-sized amphibious arvicolines, Neofiber and Arvicola (Fig. 2A). This relationship might reflect a similar structural or functional grade for the three taxa. Willam A. Akersten of the Los Angeles County Museum (personal communication) stated that the post- 451 288 JOURNAL OF MAMMALOGY Vol. 55, No. 2 A 10 5 0 5 10 5 20 25 Length of molar row Greatest length of skull Basal Basilar Pliopotamys Neofiber Palatal Palitar Ondatra Diastema Palatal bridge Width of brain case Zygomatic breadth Width of rostrum Least interorbital breadth Length of molar row Greatest length of skull Neofiber Basal Basilar Palatal Microtus Neotoma Palitar Diastema Palatal bridge Width of brain case Zygomatic breadth Width of rostrum Least interorbital breadth 25 20 15 Te) 5 O 5 10 B Fic. 2.—Ratio diagrams modified from Simpson et al. (1960) comparing various cranial measurements of six rodent genera. Logs of the means of dimensions in Neofiber alleni are assumed to be zero, while the differences between the log of the mean in N. alleni and the species being compared are plotted to the positive (+) or negative (—) sides of the zero line. A, comparison of N. alleni to Arvicola terrestris, Ondatra zibethicus, and Pliopotamys minor. B, comparison of N. alleni to Microtus ochrogaster and Neotoma cinerea. cranial skeleton of P. minor exhibits aquatic adaptations similar to Neofiber, and that Ondatra is much better adapted to an aquatic existence than either of the other taxa. The curve (Fig. 2A) for Ondatra only loosely corresponds to any of the other taxa. The curve (Fig. 2B) for Neotoma cinerea (a ter- restrial cricetine) parallels that of Microtus ochrogaster (a terrestrial arvic- oline). The relationship suggests, again, that the curves are reflecting a similar structural or functional grade of the taxa that are compared. The similarities between Pliopotamys and Arvicola are most likely due to parallelism, as Kowalski (1970) indicated that Arvicola has evolved from 452 May 1974 ZAKRZEWSKI—FOSSIL ONDATRINI 289 Mimomys, the most common of the European fossil genera. The similarities between Pliopotamys and Neofiber could also represent parallelism. Recently Hibbard (personal communication ) has redescribed an ondatrine from Kansan deposits in Texas which he considers to be ancestral to Neofiber. The rela- tionship of this new ondatrine to Pliopotamys has not been established. Per- haps the two lines diverged from a common ancestor prior to the attainment of the Pliopotamys grade, or the Neofiber lineage might have evolved from Plio- potamys fairly early in the history of the group and remained relatively con- servative in its aquatic adaptations. SPECIMEN FROM ARIZONA The ondatrine from Arizona is at an intermediate stage of evolution be- tween Pliopotamys meadensis from the Dixon local fauna (Nebraskan) of Kansas and Ondatra idahoensis from the Grand View local fauna (Aftonian) of Idaho. This assumption is based on the relative development of the den- tine tract on the lingual side of the first alternating triangle on the upper first molar. There is also a dentine tract on the posterior surface of the posterior loop of the upper third molar on the specimen from Arizona, which is not found in P. meadensis. Roots of the teeth in the ondatrine from Arizona are not as developed as those of Pliopotamys minor, based on the configuration of that portion of the maxillary that contains the alveoli. This area is intermediate in development between that found in P. minor and Neofiber. The median area of the palate in the specimens from Arizona does not have a ridge, and thus resembles the median area of the palate in Ondatra. However, possibly the palate was dam- aged. The specimen from Arizona probably represents a new species of arvic- oline, but the absence of specimens in advanced stages of ontogenetic develop- ment makes even generic assignment difficult at this time. Hibbard’s (1959) discussion of the importance of dentine tracts in the tax- onomy of ondatrines apparently has led to the misconception among some workers (for example, Shotwell, 1970) that Pliopotamys is separated from Ondatra chiefly by the former’s lack of well-developed dentine tracts. Al- though there is a high correlation in the taxa thus far described between poorly-developed or no dentine tracts in Pliopotamys and well-developed den- tine tracts in Ondatra, this is not the chief basis for separation of the two forms. The chief character by which the two genera are separated is the presence or absence of cement in the re-entrant angles. Cement is present at sometime in the ontogeny of an individual in Ondatra and absent in Pliopotamys. In addition to the lack of cement and shorter dentine tracts, Pliopotamys is gen- erally smaller and has better developed roots. However, if Pliopotamys is ancestral to Ondatra (as Hibbard and I believe) then a continuum, or tem- poral cline, in these parameters should exist that will document the evolu- tionary change of one genus into the other. 453 290 JOURNAL OF MAMMALOGY Vol. 55, No. 2 Clines within these genera have been demonstrated (Semken, 1966; Zakr- zewski, 1969), as has overlap in size between the two (Zakrzewski, 1969: fig. 11). Therefore, the presence or absence of cement in these intermediate forms would appear to be the best criterion for taxonomic assignment at the generic level. However, a problem exists even with this parameter; as first pointed out by Hibbard (1959), in primitive species of Ondatra cement is not formed in the re-entrants until well into the adult or old adult stages. I believe the development of the dentine tract in the ondatrine from Arizona to be almost intermediate between those of the most advanced species of Plio- potamys and the most primitive species of Ondatra so far known, but the in- dividual is only in the young adult stage of ontogenetic development; there- fore, I do not know to which of the above two ondatrine genera the specimen should be assigned. A similar problem exists with the specimen that Hibbard (1959) assigned to Ondatra from the Borchers local fauna (Aftonian) of Kansas. This specimen (an isolated lower first molar) is immature and lacks cement in the re-entrant angles. However, in the development of dentine tracts and size it compares favorably with individuals of O. idahoensis from the Grand View local fauna of Idaho and is correctly assigned. Because of the stage of evolution of the specimen from Arizona and the fact that it was not found at the type locality of the Benson local fauna (late Pliocene), I thought it might be a member of a younger local fauna that in- habited the area subsequent to the Benson local fauna. However, Dr. Rich- ard H. Tedford of the American Museum of Natural History (written com- munication) stated that, based on field work by Ted Galusha, the site from which the specimen was obtained is at the same stratigraphic level as the type locality of the Benson local fauna, and that both sites are well below the lowest Curtis Ranch local fauna sites of middle Pleistocene age. These facts suggest that an early radiation of the Ondatrini occurred in the Ameri- can southwest. Hibbard (1959) and Bjork (1970) suggested that Pliopotamys might have been a western form until mountain glaciation resulted in their movement onto the plains in the Pleistocene. The Benson local fauna is considered to be approximately temporally equiv- alent to the Rexroad local fauna of southwestern Kansas, whereas the Hager- man local fauna is considered to be no older than the former two and prob- ably slightly younger, but still late Pliocene in age (Zakrzewski, 1969). If these temporal associations are correct, then the relationship between Plio- potamys minor from the Hagerman local fauna and the ondatrine from the Benson local fauna is another example of a more primitive member of a lin- eage being present in the former fauna and a more advanced member in the latter fauna. I (1969) reported the presence of a pocket gopher with rooted teeth, Pliogeomys parvus, from the Hagerman local fauna, whose character- istics, with the exception of roots and size, are similar to those of Geomys 454 May 1974 ZAKRZEWSKI—FOSSIL ONDATRINI 291 minor, the type of which was described by Gazin (1942) from the Benson local fauna. Pliopotamys is not known from the Rexroad local fauna, but Ogmodontomys, which is present, might have been its ecological equivalent. The latter genus becomes extinct on the plains shortly after the appearance of Pliopotamys. SPECIMENS FROM CALIFORNIA When I examined these specimens a few years ago, the presence of a well- developed fourth triangle on UCMP 57958 suggested that the tooth might be assignable to the genus Pliopotamys. The specimens from California ap- proach Pliopotamys in length of re-entrant angles and width of tooth; how- ever, the occlusal length is much shorter and the enamel is thinner. In UCMP 57958 the fourth alternating triangle is triangular rather than knob-like, as in most of the four-triangled Cosomys from UM-Ida.la-65 of the Hagerman local fauna (Zakrzewski, 1969: fig. 7E). Nor is there any modification of the alternating triangle into a prism fold or enamel ridge as is generally found in C. primus. The third external re-entrant angle does not appear to be very deep, but, as the specimen is broken just anterior to this point, not much cer- tainty can be attached to this observation. UCMP 32952 resembles Cosomys in that it possesses an enamel ridge on the fourth triangle. The ondatrines from California are much more robust than the four-triangled Cosomys from UM-Ida.la-65. They are about the length of the three-triangled Cosomys from the other localities, but the width of UCMP 57958 falls outside the ob- served range of 252 measured specimens. The type of C. primus compares more favorably with the three-triangled Cosomys from the Hagerman local fauna. The two specimens from California appear to be more closely related to each other (on the basis of thinness of enamel and the development of re- entrant angles, which are long and narrow) than either is to Pliopotamys or Cosomys. UCMP 57958 is much wider than UCMP 32952, but this may be due to ontogenetic differences between the individuals. Possibly these speci- mens represent another species of Cosomys that was more advanced than C. primus, or a small species of Pliopotamys, or another genus of arvicoline. The imperfect condition of the specimens precludes a definitive judgement at this time. ACKNOWLEDGMENTS For the loan of and permission to publish on specimens in their care, I am indebted to John A. White (Museum, Idaho State University), Richard H. Tedford (Division of Verte- brate Paleontology, American Museum of Natural History), and Donald E. Savage (Mu- seum of Paleontology, University of California). I thank Jerry R. Choate (Museum of the High Plains, Fort Hays Kansas State College) and Claude W. Hibbard (Museum of Pa- leontology, University of Michigan) for the loan of specimens in their care and for critically reading the manuscript. David P. Whistler (Division of Vertebrate Paleontology, Los 455 292 JOURNAL OF MAMMALOGY Vol. 55, No. 2 Angeles County Museum of Natural History) made available the type of Cosomys primus for study. The drawings were penciled by Lisa Hansen (Idaho State University). This study began at Idaho State University while I was on a Postdoctoral Fellowship sponsored jointly by Idaho State University and the Los Angeles County Museum of Natural History (NSF- GB5116). LITERATURE CITED Byork, P. R. 1970. The carnivora of the Hagerman local fauna (late Pliocene) of south- western Idaho. Trans. Amer. Phil. Soc., n.s., 60:1-54. Gazin, C. L. 1942. The late Cenozoic vertebrate faunas from the San Pedro Valley, Ariz. Proc. U.S. Nat. Mus., 92:475-518. Hersuxovitz, P. 1962. Evolution of neotropical cricetine rodents (Muridae), with special reference to the phyllotine group. Fieldiania: Zool., 46:1-524. Hreparp, C. W. 1959. Late Cenozoic microtine rodents from Wyoming and Idaho. Papers Michigan Acad. Sci., Arts and Letters, 44:3-40. Hipparp, C. W., anv R. J. ZAKRZEWSKI. 1967. Phyletic trends in the late Cenozoic microtine Ophiomys gen. nov., from Idaho, Contrib. Mus. Paleo., Univ. Mich- igan, 21:255-271. Kowatskt, K. 1970. Variation and speciation in fossil voles. Symp. Zool. Soc. London, 26:149-161. Kretzor, M. 1969. Skizze einer Arvicoliden—Phylogenie—Stand 1969. Vert. Hung., Mus. Nat. Hist. Hung., 11:155-193. Quay, W. B. 1954. The anatomy of the diastemal palate in microtine rodents. Misc. Publ. Mus. Zool., Univ. Michigan, 86:1-41. SEMKEN, H. A., Jr. 1966. Stratigraphy and paleontology of the McPherson Equus Beds (Sandahl local fauna), McPherson County, Kansas. Contrib. Mus. Paleo., Univ. Michigan, 20:121-178. SHOTWELL, J. A. 1970. Pliocene mammals of southeast Oregon and adjacent Idaho. Bull. Mus. Nat. Hist., Univ. Oregon, 17:1-103. Srmupson, G. G., A. Roe, anp R. C. Lewontin. 1960. Quantitative Zoology. Harcourt, Brace, and World Inc., New York, rev. ed., 440 pp. Witson, R. W. 1932. Cosomys, a new genus of vole from the Pliocene of California. J. Mamm., 13:150-154. ZAKRZEWSKI, R. J. 1969. The rodents from the Hagerman local fauna, upper Pliocene of Idaho. Contrib. Mus. Paleo., Univ. Michigan, 23:1-36. Sternberg Memorial Museum and Department of Earth Sciences, Fort Hays Kansas State College, Hays, 67601. Submitted 6 April 1973. Accepted 29 August 1973. 456 88 PROC. S. D. ACAD. SCI. XLIV (1965) TYPE LOCALITIES OF COPE’S CRETACEOUS MAMMALS Robert W. Wilson Museum of Geology South Dakota School of Mines and Technology, Rapid City ABSTRACT It is generally stated in paleontological literature that J. L. Wortman found the types of two species of Late Cretaceous mammals in unknown parts of South Dakota. These species, subsequently described and named by E. D. Cope, are Meniscoessus conquistus (probably the first Cretaceous mam- mal to be found and described), and Thalaeodon padanicus. They are the only Cretaceous mammals of published record from the state. Review of some neglected sources of information leads to the conclu- sion that: (1) the type of Meniscoessus conquistus came from Dakota Terri- tory, but not necessarily from South Dakota, and (2) E. D. Cope, rather than Wortman, found the type of Thlaeodon padanicus, and this specimen came from Hell Creek beds along the Grand River approximately four miles south- east of Black Horse. E. D. Cope named and described two genera of Cretaceous mam- mals: these were the multituberculate Meniscoessus in 1882, and the marsupial Thlaeodon in 1892, with type species M. conquistus and T. padanicus respectively. Cope credited J. L. Wortman with the discovery of Meniscoessus conquistus, but said nothing about the type locality. In his description of Thlaeodon padanicus, he said nothing about either the discoverer or the place of discovery, except to state that the upper and lower jaws were found about one hun- dred feet apart, but probably pertained to a single individual. At a considerably later time, G. G. Simpson (1929) and others have stated that the type specimens of both M. conquistus and T. padanicus were found by Wortman in the “Laramie” [Lance] of South Dakota, but that no other locality data were available. The Museum of Geology of the South Dakota School of Mines and Technology has been exploring the Hell Creek (Late Cretaceous) of South Dakota for mammals.’ In an attempt to gain clues as to where Wortman might have found his specimens, I searched such literature as was available to me with care. As a result, I have reached tentative conclusions at variance with those of Simpson. In respect to Meniscoessus conquistus not much can be said with assurance. A note by Wortman (1885, p. 296) states that Hill (Rus- sell?) and Wortman found the type in the summer of 1883 (sic, but ‘Work supported by National Science Foundation grant G23646 457 PROC. S. D. ACAD. SCI. XLIV (1965) 89 surely 1882) in Dakota. Because the division of the Territory into the present states of North and South Dakota did not take place until 1889, the question arises as to how it is known that the locality was in what is now South Dakota if nothing is known about the de- tails of the locality. The only slight clue I can uncover is that a year after Wortman’s finding of Meniscoessus, Cope, himself, was explor- ing the Cretaceous of the Dakota Territory. In a letter to his wife dated August 28, 1883 (Osborn, p. 306), and written at what is seem- ingly now Medora, North Dakota, he says in describing local out- crops: ‘This is the formation from which Wortman got the Menis- coessus.” This sentence can be taken literally as simply that the specimen came from Cope’s Laramie Formation, or with more license that he meant these are the outcrops from which the specimen came. In the same letter, he wrote that he planned to go 30 miles south where the “badlands are said to be exceptionally bad.” If he were following Wortman’s footsteps at this point, he would have been approximately 45 miles north of the state line. After proceed- ing this far south along the Little Missouri, Cope went southeast- ward to White Buttes before turning back to Medora. White Buttes was his closest approach to South Dakota on this trip of several days, and he was then still about 30 miles from South Dakota. It may be that in the general area bounded by Medora, Marmath, and Bowman, North Dakota, Wortman found the type of Meniscoessus, but even if he did not, it is highly uncertain that the discovery was made in the South Dakota of today. As a matter of fact, most of the outcrops south of the state line for some miles may be somewhat too high in the geologic section for Meniscoessus. In respect to the type locality of Thlaeodon padanicus, there are several bits of evidence suggesting (1) that Cope rather than Wort- man found the specimen, and (2) that it was in fact found in South Dakota along the south bank of the Grand River southeast of Black Horse. These lines of evidence are itemized below. 1. Nowhere in the account published in 1892 in the American Naturalist does Cope credit Wortman with discovery of Thlaeodon padanicus. 2. The Indian name for the Grand River is Padani, and hence the specific name T. padanicus is a broad hint as to locality. 3. In the year of its discovery, Cope prospected along the Grand River. Wortman was also in South Dakota, but was occupied by collecting in the Big Badlands to the south, and such Cre- taceous collections as he made seemed to have been in the Lance Creek area of Wyoming. In any case, even before the summer of 1892, he had left the employ of Cope, and was working for the American Museum of Natural History. 458 90 PROC. S. D. ACAD. SCI. XLIV (1965) 4. In a letter to his wife dated July 17, 1892 (Osborn, p. 431), Cope says, ‘‘We made noon camp on the bank of Grand R. and then climbed the bluffs on the S. side leaving the Rock Creek and this subagency to the N. We followed this high land, driving through the Grass, sometimes with, sometimes with- out trail. We had great distance views, fine air, and plenty of flowers. During the afternoon we crossed Five (sic, for Fire) Steel Creek, which comes in from the South. As evening approached thunderclouds arose in the W. and I began to think of camp. Oscar however drove on, and the Sioux boy kept ahead. As it grew late we turned down a low hill to the left and climbed a low bench at the foot of an opposite hill. I saw a low bare bank and lying around white objects. I told Oscar to let me get out, as I thought I saw bones. Sure enough the ground was covered with fragments of Dinosaurs, small and large, soon we found water and stopped for camp.” ingly thought; see 1931, p. 415). 5. In the letter above-mentioned (Osborn, p. 443), Cope states his results as, “In the 3 days I collected I got 21 species of vertebrates, of which 3 are fishes, and all the rest reptiles except one mammal. This is a fine thing, the most valuable I procured, and new as to species at least; and it throws im- portant light on systematic questions.” This mammalian specimen is not otherwise accounted for in collections if it is not the type specimen of T. padanicus (as H. F. Osborn seem- Reference to a geological map (Firesteel Creek Quadrangle, South Dakota State Geological Survey) shows that the closest ex- posures from whence these bones could come after the Firesteel crossing is in the vicinity of section 25, T. 20N, R. 22E, or sections 29 and 30, T. 20N, R. 23E. A good skeleton of Anatosaurus in the Mu- seum of Geology collections is from the southwest corner of the SW’, of section 25, T. 20N, R. 21E. The type of Thlaeodon padanicus surely came from somewhere in the area of these localities. LITERATURE CITED Cope, E. D., 1882, Mammalia in the Laramie Formation. Amer. Nat., v. 16, pp. 830-831. , 1892, On a New Genus of Mammalia from the Laramie Formation. Amer. Nat., v. 26, pp. 758-762, pl. xxii. Osborn, H. F., 1931, Cope: Master Naturalist. Princeton Univ. Press, xvi plus 740 pp., 30 figs. Princeton. Simpson, G. G., 1929, American Mesozoic Mammals. Mem. Peabody Mus. Yale Univ., v. 3, pt. 1, xv plus 235 pp., 62 text-figs., 32 pls. Wortman, J. L., 1885, Cope’s Tertiary Vertebrata. Amer. Jour. Sci. (3), v. 30, pp. 295-299. 459 THE ADAPTIVE RADIATION OF THE PHENACODONTID CONDYLARTHS AND THE ORIGIN OF THE PERISSODACTYLA! LEONARD B. RADINSKY Department of Biology, Brooklyn College, Brooklyn, New York Accepted March 28, 1966 The mammalian order Condylarthra in- cludes a heterogeneous assemblage of small- to medium-sized archaic omnivores and herbivores. Most families in the order flourished in the Paleocene and became extinct early in the Eocene. A few lineages, however, developed crucial adap- tations which led to their emergence as new orders of mammals, one of which was the Perissodactyla. The origin of the Perissodactyla is better documented than that of any other order of mammals and provides an excellent opportunity to study the emergence of a major taxon. Dental evidence indicates that perisso- dactyls were derived from the condylarth family Phenacodontidae. To view in proper perspective the evolutionary changes which led to the origin of the Perissodactyla, it will be necessary to survey the adaptive radiation of the Phe- nacodontidae. The oldest true phenacodontid condy- larth, Tetraclaenodon, first appears in faunas of middle Paleocene age, and by the beginning of the late Paleocene ap- pears to have radiated into three main groups, represented respectively by Phe- nacodus, Ectocion, and an as yet unknown proto-perissodactyl. Forms transitional be- tween Tetraclaenodon and Phenacodus (primitive species of Phenacodus), and between Tetraclaenodon and _ Ectocion (the genus Gidleyina) are known, but no intermediates between Tetraclaenodon and the most primitive known perissodacty]l, the early Eocene genus Hyracotherium, have yet been found. However, Tetraclae- nodon is the most advanced form which is 1 This work was supported in part by National Science Foundation Grant GB-2386. Evotution 20: 408-417. September, 1966 still unspecialized enough to have given rise to Hyracotherium. (The occurrence of incipient mesostyles in a small number of Tetraclaenodon specimens does not preclude this possibility; the alternative hypothesis, that proto-perissodactyls and Tetraclaenodon were independently de- rived from a still more primitive common ancestor, requires an additional compli- cating factor—an independent acquisition of molar hypocones by perissodactyls and phenacodontids.) Thus, in the absence of evidence to the contrary, Tetraclaenodon may be considered directly ancestral to perissodactyls. The major morphological changes involved in the evolution of the Tetraclaenodon stock into Phenacodus, Ectocion, and Hyracotherium, fall into two functional categories, one concerned with mastication and the other with loco- motion. MASTICATION Dentition The main changes involved in the evo- lution of the phenacodontid dentition oc- cur in the molar teeth. The molars of Tetraclaenodon (see Fig. 1) are low- crowned, with low, obtuse cusps. The first and second upper molars are ad- vanced over the primitive tritubercular molar pattern by the addition of a fourth main cusp, the hypocone. There are two relatively large intermediate cuspules, the protoconule and metaconule, and broad anterior and posterior cingula. The third upper molar is smaller than the second and lacks a hypocone. In the lower molars the paraconid has been reduced, leaving two main anterior cusps, the pro- toconid and metaconid, and a prominent anterior ridge, the paralophid. There are 408 460 ORIGIN OF PERISSODACTYLS Fic. 1. Phenacodus. Lower molars of Ectocion and Phenaodus have the same basic cusp pattern as is seen in Tetraclaenodon and are therefore omitted. All about x 3. Abbreviations: 409 Second and third molars of A. Ectocion, B. Hyracotherium, C. Tetraclaenodon, and D. HY, hypocone; HCLD, hypoconulid; MCL, metaconule; MES, mesostyle; MLH, metaloph. three posterior cusps, a large hypoconid and slightly smaller entoconid and hypo- conulid. The third lower molar is nar- rower posteriorly than the second. The wear facets on the molars of Tetraclaeno- don suggest that both crushing and shear- ing occurred in mastication, with the em- phasis apparently on crushing. The teeth of Phenacodus are very sim- ilar to those of Tetraclaenodon, having low, obtuse cusps and ridges. The main differences are the development of a small mesostyle on the upper molars and the enlargement of the posterior cingulum into a hypocone on the third upper molar. The upper molars are relatively long (antero- posteriorly) and narrow. As in Tetraclae- nodon, the broad low cusps are more adapted for crushing than shearing. The addition of a hypocone on the third upper molar increases the surface area available for chewing. The mesostyle is not large 461 410 enough to add significantly to the ecto- loph area. In molars of Lctocion the cusps are relatively higher and more acute and the ridges connecting cusps are more promi- nent than in Tetraclaenodon or Phenaco- dus. The ectoloph is higher relative to the lingual cusps and is folded into a prom- inent mesostyle. The upper molars are relatively short and wide. The third up- per molar does not develop a hypocone. On the lower molars the paraconid is lost and the paralophid no longer extends to the metaconid (as it does in Phenacodus). The high, narrow cusps and ridges provide steep occlusal surfaces, indicating rela- tively more shear and less crushing than occurred in Tetraclaenodon or Phenaco- dus. The prominent mesostyle increases the length of ectoloph available for ver- tical shear against the labial sides of ridges on the lower molars. The molars of AHyracotherium, like those of Ectocion, have relatively higher and more acute cusps and ridges than do those of Tetraclaenodon or Phenacodus. However, Hyracotherium is even more advanced in this respect than is Ectocion, for the crests connecting cusps are better developed. An important modification in cusp pattern has been brought about by the loss of the protcone-metaconule con- nection, an anterior shift of the meta- conule and the development of a hypo- cone-metaconule crest. These changes re- sult in a cusp pattern with two oblique tranverse crests (an anterior protoloph and posterior metaloph) separated by a lingually open valley. Correlated with the changes in upper molar pattern, in the lower molars the hypoconulid has been posteriorly displaced, leaving the posterior sides of the hypoconid and equally large entoconid clear for shear against the ante- rior side of the metaloph above. Another new feature in the dentition of Hyracothe- rium is the enlargement of the third molars. In Hyracotherium the upper third molar has a hypocone and is as large as the second molar. The third lower molar is larger than the second, owing to the LEONARD B. RADINSKY great enlargement of the hypoconulid. (In the first and second lower molars the hypoconulid is reduced.) However, even excluding the enlarged hypoconulid, the third lower molar is still as large as the second. Finally, the lower molars of Hyracotherium are narrower relative to the uppers than is the case in the phe- nacodontids. The changes in cusp pattern and tooth proportions in evolution from Tetraclae- nodon to Hyracotherium indicate an in- crease in the amount of shearing (espe- cially along transverse crests) and a cor- responding decrease in the amount of crushing in mastication. A shift toward increased shearing also occurred in Ecto- cion, but in that genus the emphasis was on vertical ectoloph shear. The enlarge- ment of the third molars in Hyracotherium provided greater occlusal surface and could have been brought about simply by a slight posterior shift of the molarization field. The greatly enlarged hypoconulid of the third lower molar served the function in occlusion of a paralophid and presum- ably developed in correlation with the molarization (and enlargement) of the posterior half of the upper third molar. The relatively narrower lower molars of Hyracotherium required a greater degree of transverse jaw movement for complete occlusion with the uppers than was neces- sary in Tetraclaenodon. Jaw Musculature The structure of the lower jaw, known for Phenacodus, Ectocion, and Hyracothe- rium (see Fig. 2), provides information on the relative proportions of the main com- ponents of the jaw musculature. In man- dibles of Hyracotherium the coronoid process is relatively smaller and the angle relatively larger than in Phenacodus or Ectocion. In addition, the posterior bor- der of the angle is thicker and more heav- ily scarred (from insertions of the ex- ternal masseter and internal pterygoid muscles) in Hyracotherium. These differ- ences suggest that the masseter and in- ternal pterygoid muscles were relatively 462 ORIGIN OF PERISSODACTYLS Fic. 2. (after Simpson, 1952), X 4%; B. Ectocion (Yale Peabody Mus. no. 21211), X %; C. Phenacodus (Princeton Univ. no. 14864), X 1. All in lat- eral view. Lower jaws of A. Hyracotherium larger, and the temporalis, which inserts on the coronoid process, relatively smaller in Hyracotherium than in the phenaco- dontids. In living ungulate herbivores the mas- seter-pterygoid complex is larger than the temporalis, while in carnivores the oppo- site is true (Becht, 1953, p. 522; Schu- macher, 1961, pp. 143, 180). In carni- vores, jaw movement is almost entirely confined to adduction, for which the temporalis is well suited, but in ungulates and many other herbivores transverse movement is important in mastication, and for transverse movement the deep part of the masseter and the internal pterygoid are more efficient than the temporalis (Smith and Savage, 1959, p. 297). Thus the relatively larger masseter and internal pterygoid musculature indi- cated by the jaw structure of Hyracothe- 41] rium suggests increased specialization for lateral jaw movement in mastication. This specialization of the jaw musculature cor- relates with the narrower lower molars and predominance of transverse shear in- dicated by the molar cusp patterns of Hyracotherium. LOCOMOTION Much of the postcranial skeleton is known for Hyracotherium, Phenacodus and, to a lesser degree, Tetraclaenodon, but that of Ectocion is largely unknown. Therefore the following discussion of loco- motory adaptions will deal mainly with the first three genera. Vertebral Column Slijper (1946, p. 103) pointed out that with decreasing mobility of the vertebral column in ungulates the longissimus dorsi shifts its insertion posteriorly from lum- bar to sacral vertebrae and consequently the neural spines of the lumbar vertebrae become less cranially, and even caudally, inclined. In Phenacodus copei (Amer. Mus. Nat. Hist. no. 4378) the lumbar neural spines are inclined cranially about 15 degrees from vertical. Kitts (1956, p. 21) states that the neural spine of the last lumbar vertebra of Hyracotherium is less cranialy inclined than that of Phe- nacodus. No specimen of Hyracotherium available to me preserves lumbar neural spines, but in Heptodon posticus, an early Eocene tapiroid similar in morphology to Hyracotherium, the neural spine of the last lumbar vertebrae (Mus. Comp. Zool. no. 17670) is inclined cranially about five degrees from vertical. This difference from the condition in Phenacodus sug- gests that the vertebral column in early perissodactyls was somewhat less flexible than that of Phenacodus. Kitts (1956, p. 20) states that the zygapophyses of the lumbar vertebrae of Hyracotherium are embracing, but his il- lustration (loc. cit., fig. 3) shows what appears to be a relatively flat prezyga- pophysis, similar to the condition in Phe- nacodus. 463 412 LEONARD B. RADINSKY Fic. 3. x %; B. Tetraclaenodon (composite from AMNH nos. 2468 and 2547a), & 1; C. Phenacodus (AMNH no. 2961), X 4. Forelimb In Tetraclaenodon the humerus has a prominent deltoid crest, with the deltoid tubercle located on the distal half of the shaft, and a large medial epicondyle, with an entepicondylar foramen. The proximal end of the radius is about twice as wide as it is deep (anteroposteriorly) and artic- ulates with the ulna along a wide flat facet, indicating loss of the ability to supinate. The carpus (see Fig. 3) is rela- tively low and wide, and has been called “alternating”; that is, in dorsal view the scaphoid rests partly on the magnum and the lunar partly on the unciform. The amount of overlap, however, is slight. Facets on the distal row of carpals indi- cate that there were five digits; except for the proximal head of the third metacarpal, the metacarpus is unknown. The humerus, radius, and ulna of Phe- nacodus are similar to those of Tetraclae- nodon, except that the deltoid crest of the Front feet of A. Hyracotherium (composite from Kitts, 1957, and Osborn, 1929, fig. 700), humerus is slightly weaker and the deltoid tubercle is higher on the shaft. The car- pus of Phenacodus has been described as being of the serial type, i.e., with the scaphoid resting solely on the trapezoid and trapezium, and the lunar only on the magnum. This arrangement occurs in the large species of Phenacodus, P. primaevus, but in the small species P. copei (AMNH no. 16125), the lunar overlaps the unci- form to about the same degree (which is very little) as in Tetraclaenodon. The less prominent deltoid crest and higher deltoid tubercle suggest that the forelimb of Phenacodus was relatively less powerful but perhaps capable of more rapid movement than that of Tetraclaeno- don. The small medial displacement of the lunar and scaphoid, resulting in loss of the lunar-unciform and scaphoid-mag- num articulations in large species of Phe- nacodus, suggests a slight increase in importance of the ulna in weight support. 464 ORIGIN OF PERISSODACTYLS The forelimb of Hyracotherium differs from that of Tetraclaenodon in the follow- ing features: humerus with shorter and less prominent deltoid crest and more proximally located deltoid tubercle, greatly reduced medial epicondyle (with conse- quent loss of the entepicondylar foramen), and sharper intercondyloid ridge (= capit- ulum); radiohumeral index of about 1.0 compared to 0.8 in Tetraclaenodon and Phenacodus, ulna with narrower, less mas- sive, more symmetrical olecranon; carpus relatively higher and narrower, with more extensive articulations between elements; cuneiform smaller and scaphoid displaced laterally to extensively overlap unciform and magnum, respectively; unciform, mag- num, and scaphoid with larger posterior tuberosities; first digit lost and trapezium reduced to a tiny nubbin; remaining meta- carpals relatively longer and thinner (the ratio of the length of the third metacarpal to the humerus is 1:2 compared to about 1:3 in Phenacodus and probably also Tetraclaenodon); fifth metacarpal rela- tively smaller. All of these differences indicate in- creased specialization for running in Hy- racotherium. The elongation of distal limb segments (radius and metacarpals) and reduction of lateral digits increases the length of stride and makes the limb a more effective lever. The reduction of the medial epicondyle probably correlates with the decreased importance of the pro- nator teres (which originates on that epi- condyle), for the manus is fixed in a per- manently pronated position, and may also correlate with the decrease in importance of the ulna as a weight-bearing element of the forearm. The latter change is indi- cated by the reduction in size of the cuneiform and lateral displacement of the lunar and scaphoid, which increases the relative size of the area of manus under the radius. The alternating arrangement of the carpals and more compact carpus make the wrist less flexible but better for resisting stresses. The larger posterior tu- berosities on several of the carpals indicate more powerful flexor musculature. The 413 sharper intercondyloid ridge on the hu- merus restricts lateral movement at the elbow joint. The weaker deltoid crest, higher deltoid tubercle, and narrower and less asymmetrical olecranon are features associated with increased _ cursoridlity. Thus, in a complex of features, the fore- limb of Hyracotherium is more specialized for running than is that of Tetraclaenodon or Phenacodus. Hind Limb In Tetraclaenodon the greater trochan- ter of the femur is only slightly higher than the head, the lesser trochanter is very weak, and the third trochanter is large and located about two-fifths of the way down the shaft. The cnemial crest of the tibia is relatively large and extends about halfway down the shaft, the grooves for the astragalus are broad and very shallow, and the medial malleolus and distal end of the fibula (lateral malleolus) are large and massive. The astragalus has a relatively flat, low, and wide trochlea with a foramen, a relatively long neck, and a dorsoventrally flattened, convex head. The posterior astragalocalcaneal ar- ticulation is only slightly rounded. The calcaneum has a large peroneal tubercle and the ectocuneiform a large plantar process. The pes is pentadactyl, with the lateral toes slightly reduced (see Fig. 4). The hind limb of Phenacodus is similar to that of Tetraclaenodon, differing in the following features: femur with larger lesser trochanter; tibia with weaker cne- mial crest, smaller medial malleolus, and slightly deeper grooves for astragalus; fibula relatively slimmer, with smaller dis- tal end; astragalus with a slightly rela- tively higher, narrower, and more deeply grooved trochlea, a slightly more curved posterior astragalocalcaneal facet, no as- tragalar foramen, and a deeper (dorso- plantarly) head; first and fifth metatar- sals slightly more reduced. The enlarged lesser trochanter of the femur suggests a stronger iliopsoas, an adductor of the femur. The reduction of the cnemial crest suggests reduced power 465 414 LEONARD B. RADINSKY Fic. 4. Hind feet of A. Hyracotherium (from Kitts, 1956), X %; B. Tetraclaenodon (from Mat- thew, 1897), X 1%; C. Phenacodus (AMNH no. 293), X 4. but increased speed in the hind limb. The more deeply grooved astragalar trochlea helps restrict lateral movement at the upper ankle joint and reduces the necessity for large lateral and medial malleoli. The loss of the astragalar foramen allows a slightly greater arc of rotation of the astragalus on the tibia. The more curved posterior astragalocalcaneal facet and deeper astragalar head may be related to a more digitigrade posture, which is sug- gested by the reduction of the lateral toes. In all of these features the hind limb of Phenacodus is slightly more specialized for running than is that of Tetraclaenodon. The hind limb of Ectocion is known only from an astragalus and part of a cal- caneum (AMNH no. 16127). The astrag- alus (see Fig. 5) differs from that of Tetraclaenodon in having a slightly higher and narrower tibial trochlea with a slightly deeper groove and no astragalar foramen, a more anteriorly directed posterior cal- caneal facet, a wider neck with a high anteroposteriorly oriented ridge at the dorsolateral corner, and a slightly flatter and deeper navicular facet. The high dorsolateral ridge probably marks the at- tachment of a strong lateral astragalocal- caneal ligament, which suggests restriction of rotation between astragalus and calca- neum. This interpretation is supported by the less oblique posterior calcaneal facet and the flatter head (the latter indicates less movement between astragalus and navicular). These features suggest a slight 466 ORIGIN OF PERISSODACTYLS ‘sl | if D ! Fic. 5. Astragali of A. Ectocion (AMNH no. 16127), B. Hyracotherium, C. Phenacodus, D. Tetraclaenodon. Not to scale. loss of freedom for lateral movement in the tarsus of Ectocion compared with the condition in Tetraclaenodon. The anterior end of the calcaneum is as wide in Ecto- cion as in Tetraclaenodon, suggesting that the pes of Ectocion was pentadactyl. The hind limb of Hyracotherium differs from that of Tetraclaenodon in the same features mentioned for Phenacodus, but to a greater degree and with additional mod- ifications. The latter include: femur with higher greater trochanter and more proxi- mally located third trochanter; cnemial crest of tibia does not extend as far dis- tally; first and fifth digits lost and re- maining metatarsals. relatively longer (length of third metatarsal/femur = 0.50 in Hyracotherium compared to 0.35 in the phenacodontids); tarsus relatively nar- rower and more compact, and astragalus, calcaneum, and navicular modified to eliminate the possibility of lateral move- ment of the foot. The higher greater trochanter (which provides better leverage for the gluteal muscles, important abductors of the fe- mur), more proximally located third tro- chanter, shorter cnemial crest, and longer metatarsals, plus the modifications noted in Phenacodus, are cursorial specializa- tions of Hyracotherium which occur also in other running mammals. The loss of the first and fifth toes and the great 415 elongation of the remaining metatarsals are not unusual cursorial adaptations in later forms but are extremely progressive features for an early Eocene mammal. They require a compact, relatively rigid tarsus and it is in modifications of the tarsus to provide a stable ankle joint that Hyracotherium was unique. The interpretation of tarsal mechanics in extinct animals is necessarily limited by lack of knowledge of the tarsal ligaments, for the ligaments may be as important as the bone articulations in restricting move- ment. Thus the degree of tarsal movement inferred from the bones alone represents the maximum amount possible and in life the actual amount of movement may have been considerably less. The configurations of the tarsal articu- lations in Tetraclaenodon suggest that lateral movements of the foot (eversion and inversion) were possible, resulting from a combination of rotation at the lower ankle joint (between astragalus and calcaneum) and transverse tarsal joint (between astragalus and navicular). The posterior astragalocalcaneal articulation is only gently curved and the astragalo- navicular articulation resembles a shallow ball-and-socket joint. In Hyracotherium the posterior astragalocalcaneal articula- tion is bent into a right angle and is more vertically oriented, restricting rotation at the lower ankle joint, and the astragalo- navicular articulation is saddle-shaped (with the distal end of the astragalus concave mediolaterally), allowing a small amount of dorsoplantar rotation but no lateral movement. The saddle-shaped as- tragalonavicular articulation is unique to the Perissodactyla and a diagnostic fea- ture of the order. The redistribution of weight necessi- tated by the loss of the lateral toes and relative enlargement of the middle digit in Hyracotherium is reflected in the nar- rower, more compact tarsus, in which the cuboid and calcaneum are narrower (the peroneal tubercle of the calcaneum is lost), the neck of the astragalus shorter, wider, and deeper, and the head more 467 416 closely appressed to the calcaneum, and the entocuneiform reoriented so that the vestigial first metatarsal is located behind the ectocuneiform and third metatarsal where it serves as attachment for deep flexor muscles and as a brace for the tarsus (Radinsky, 1963). The plantar process of the ectocuneiform is lost, its function apparently having been usurped by the reoriented vestige of the first meta- tarsal. Thus virtually the whole tarsus of Hyracotherium was remodeled to provide the stability required by the loss of lateral toes and great elongation of the metatar- sus. Versatility was sacrificed for in- creased efficiency in running. DISCUSSION Absolute dating of the early Tertiary (Evernden e¢ al., 1964) indicates that evolution from Tetraclaenodon to Hyraco- therium took place in less than five mil- lion years. Considering the magnitude of the morphological changes involved, the speed of that transition indicates a con- siderably higher rate of evolution in late Paleocene proto-perissodactyls than oc- curred during most of the subsequent 55 million years of perissodactyl evolution. This fact, coupled with the evidence of a major adaptive radiation of perissodactyls at the beginning of the Eocene, suggests that the origin of the Perissodactyla coin- cided with a shift to a new adaptive level. The two major areas of specialization of the earliest perissodactyls, as far as the paleontological evidence indicates, are in mastication and locomotion, and there is evidence of experimentation among the condylarths in both of these fields. The dentition of Phenacodus is essentially a conservative continuation of the basic Tetraclaenodon pattern, while that of Ec- tocion is specialized for vertical shear. The molars of Ectocion are more special- ized for vertical shear than are those of Hyracotherium, but are less specialized for transverse shear. In the closely re- lated meniscotheriid condylarths, Menisco- therium has teeth which are more special- ized for vertical shear than those of Hy- LEONARD B. RADINSKY racotherium and at least as specialized, although in a somewhat different way, for transverse shear. The specialization for transverse shear is also reflected in the mandible of Meniscotherium, which has a relatively large angular process and small coronoid process. This experimentation in dentition among condylarths suggests that a variety of ecological niches for medium- sized browsers was open at the beginning of the late Paleocene. Phenacodus, Ectocion, and Meniscothe- rium appear to have been only slightly more specialized for running than was Tetraclaenodon, although the astragalus of Ectocion suggests that lateral move- ment at the ankle joint may have been restricted by ligaments. In Hyracothe- rium, however, a radical and unique re- modeling of the ankle joint prevented lat- eral movement and made possible a pre- cocious elongation of the metatarsals and reduction of the lateral digits. Other spe- cializations for running are evident in the forelimb of Hyracotherium. During the early Eocene perissodactyls underwent an extensive radiation while phenacodontid and meniscotheriid condyl- arths became extinct. Since the menisco- theriid dentition was at least as specialized for shear as was that of Hyracotherium it would seem that the masticatory special- ization was less important for the success of the Perissodactyla than the adaptations for running. The early perissodactyls were considerably more specialized for running than were the contemporary predators, while the condylarths were not. It is surely no coincidence that the other ma- jor order of medium-sized to large herbi- vores, the Artiodactyla, appeared at the same time as the Perissodactyla, with their main adaptive feature a cursorial modifi- cation of the ankle joint (see Schaeffer, 1947). Thus it would seem that predator pressure, resulting in a major cursorial specialization, was the critical selective force involved in the origin of the Perisso- dactyla. Unfortunately there is no direct evidence of the ecological factors involved, for the faunas in which the condylarth- 468 ORIGIN OF PERISSODACTYLS perissodactyl transition took place have not yet been discovered. The absence of perissodactyls in known late Paleocene faunas and their sudden appearance in abundance at the beginning of the Eocene suggests migration from an unknown area. Thus early perissodactyls may have origi- nated isolated from, and perhaps under different selective pressures than, other descendant lineages of the middle Paleo- cene Tetraclaenodon stock. SUMMARY The middle Paleocene phenacodontid condylarth genus Tetraclaenodon gave rise to three late Paleocene groups, represented by Phenacodus, Ectocion, and an as yet unknown proto-perissodactyl. The main morphological changes indicated by the fossil evidence of this evolutionary radia- tion are specializations for mastication and locomotion. Molars of Phenacodus are very similar to those of Tetraclaeno- don, with low broad cusps apparently mainly adapted for crushing. Teeth of Ectocion have prominent W-shaped ecto- lophs, an adaptation for vertical shear, while molars of Hyracotherium, the most primitive known perissodactyl, are spe- cialized for both vertical and transverse shear. Phenacodus and Ectocion show little specialization for running over the primitive ambulatory condition of Tetra- claenodon, but the limbs of Hyracotherium display major cursorial modifications, in- cluding a unique remodeling of the ankle 417 which prevented lateral movement at that joint and made possible a_ precocious elongation and narrowing of the meta- tarsus. LITERATURE CITED Becut, G. 1953. Comparative biologic-ana- tomical researches on mastication in some mammals. Proc. Kon. Nederl. Akad. We- tensch., (C) 56: 508-527. EVERNDEN, J. F., D. E. Savacr, G. H. Curtis, AND G. T. JaMeEs. 1964. Potassium-argon dates and the Cenozoic mammalian chronol- ogy of North America. Amer. Jour. Sci., 262: 145-198. Kitts, D. 1956. American Hyracotherium (Pe- rissodactyla, Equidae). Bull. Amer. Mus. Nat. Hist., 110 (1): 5-60. MattHew, W. D. 1897. A revision of the Puerco fauna. Amer. Mus. Nat. Hist. Bull., 9 (22): 259-323. Osporn, H. F. 1929. Titanotheres of ancient Wyoming, Dakota, and Nebraska. U.S. Geol. Surv. Monograph 55 (2 vols.): 1-953. Rapinsky, L. B. 1963. The perissodactyl hal- lux. Amer. Mus. Novit., 2145: 1-8. SCHAEFFER, B. 1947. Notes on the origin and function of the artiodactyl tarsus. Amer. Mus. Novit., 1356: 1-24. ScHUMACHER, G. H. 1961. phologie der Kaumuskulatur. Jena, 262 pp. Smpson, G. G. 1952. Notes on British hyra- cotheres. J. Linn. Soc. Zool., 42: 195-206. SLijPER, E. J. 1946. Comparative biologic-an- atomical investigations on the vertebral col- umn and spinal musculature of mammals. Verh. Konink. Nederl. Akad. Wetensch. afd. Natuurk., (2) 42: 1-128. SMITH, J. M., ano R. J. G. SAVAGE. mechanics of mammalian jaws. Rev., 141: 289-301. Funktionalle Mor- G. Fischer, 1959. The School Sci. 469 GRADES AND CLADES AMONG RODENTS ALBERT E. Woop Biology Department, Amherst College, Amherst, Massachusetts Accepted September 30, 1964 As has been pointed out many times, the rodents are the most abundant and suc- cessful mammalian order. Their evolution has been channeled into a single major di- rection by the development, as an initial modification, of ever-growing, gnawing in- cisors, with associated changes in skull and jaw muscles. Subsequent evolution has in- volved a great deal of parallelism within the order, making it very difficult to dis- entangle the convergent and parallel changes from those that are truly indicative of phyletic relationship. The similarity in complexity of the evolutionary pathways among rodents to those among actinopteryg- ians, and particularly teleosts, has also been pointed out. Work by various authors has indicated that the evolution of the actinopterygians consists of the sequential attainment of a series of morphological stages, or grades (as in Huxley, 1958), each of which has been derived from the preceding one sev- eral independent times by a series of paral- lel trends. The classification of actinopts at the supraordinal level involves a series of taxa that are currently agreed to rep- resent such polyphyletic grades rather than monophyletic units or clades (Schaeffer, 1956, p. 202). The rodents were, classically, divided into three suborders on the basis of the structure of the jaw musculature and as- sociated osteological differences—the Sciur- omorpha, Myomorpha, and_ Hystrico- morpha (Simpson, 1945). All recently pro- posed classifications of the order (Lavocat, 1956; Schaub, 1958, p. 691-694; Simpson, 1959; and Wood, 1955a and 1959), adopt the multiplicity of major groups postulated by Miller and Gidley (1918) or Winge (1924), and agree that the three classic suborders are not monophyletic clades, but rather, taken as a whole, represent a grade Evotution 19: 115-130. March, 1965 that is an advance over the primitive ro- dent grade. The classic suborders repre- sent alternative expressions of an advanced rodent grade, and may well have been achieved approximately simultaneously. The various clades within the order are still not clearly recognizable, and much work remains to be done before rodent cladal classification is stabilized to every- one’s satisfaction, though considerable progress is being made. There is no direct evidence as to the type of jaw muscles in the still unknown ancestral rodents that lived during the Paleocene. However, Edgeworth (1935, pp. 73-75), in discussing the primitive mammalian jaw musculature, indicates that a major part of it consists of an em- bryological single muscle mass, divisible into the Temporalis, Zygomaticomandibul- aris, and Masseter. The Zygomaticomandi- bularis is usually divided into anterior and posterior portions by the masseteric nerve. The masseter may be single or be divisible into two or more layers, with no clear in- dications as to which is the primitive con- dition. Among students of rodent anatomy there have been many varying interpretations of the jaw musculature. Usually, the Zygo- maticomandibularis has been considered to be part of the masseter (Masseter medialis of Tullberg, 1899, pp. 61-62; Masseter profundus of Howell, 1932, pp. 410-411), but sometimes it is treated as a separate muscle (Lubosch, 1938, p. 1068; Miiller, 1933, pp. 14-24). The two parts of the masseter of Edgeworth are the Masseter lateralis superficialis and Masseter lateralis profundus of Tullberg, or the Masseter super ficialis and Masseter major of Howell. Lubosch (1938, fig. 930) and Miller (pp. 19-20) also consider the anterointernal portion of what is usually called the mas- 115 470 116 seter to be a distinct muscle, the Mavxillo- mandibularis. In the following discussion, the masseter is considered to consist of three parts— the Masseter superficialis, arising from the anterior end of the zygoma or the side of the snout and inserting on the ventral border of the angle (= Masseter lateralis superficialis); the Masseter lateralis, aris- ing from most of the length of the lateral surface of the zygoma and inserting on the ventral part of the angular process (= Masseter lateralis profundus; Masseter major); and the Masseter medialis, arising from the medial side of the zygoma, whence it has sometimes spread to the medial wall of the orbit or forward through the infra- orbital foramen, and inserting on the dor- sal portion of the masseteric fossa of the jaw (= Masseter profundus; Zygomatico- mandibularis; Maxillomandibularis). These are illustrated in Figs. 1-4. The separation of evolutionary grades among the rodents can best be done on the basis of: (1) the incisor pattern and structure; (2) the structure of the jaw muscles and the associated areas of the skull and jaws; and (3) the general pat- tern and height of crown of the cheek teeth. These can be used as general clues to evolutionary grades throughout the order. The discussion below will largely be limited to these sets of criteria. On the other hand, the separation and identifica- tion of the clades must involve the use of all available data, and must not select one set of structures as the most critical one, with other criteria neglected. GRADE ONE—PROTROGOMORPH RADIATION The initial recorded rodent radiation, known from the Eocene but presumably having gotten well started in the later Paleocene, involved animals that had al- ready acquired the basic gnawing adapta- tions. The incisors were ever-growing, with the enamel limited to an anterior band, giving the perpetual chisel-edge that characterizes the Rodentia. The upper incisor was re- ALBERT E. WOOD curved, the worn surface being nearly ver- tical, and the lower incisor acted against it by moving upward and forward. The enamel cap had extended around the edges of the incisor, on both medial and lateral faces, to brace it better against the stresses of gnawing. The incisor enamel is of con- stant distribution on the incisor cross sec- tion, once the animal reached its adult size. Histologically, the incisor enamel in the Eocene members of the group is of the type called pauciserial by Korvenkontio (1934, p. 97, and fig. 1), in which the enamel is made up of irregular bands, rang- ing from a single row of enamel prisms, to as many as three or four rows of prisms. A change to the uniserial type of enamel (op. cit., p. 130) has taken place in mem- bers of this radiation by the Oligocene. As in all known rodents, there were no pre- or postglenoid processes, the glenoid fossa being elongate and slightly inclined from rear to front, so that the jaw could be moved backward bringing the cheek teeth into occlusion, or forward bringing the incisors together and separating the cheek teeth, vertically. The dental formula had been reduced to the most primitive that is still found in liv- ing rodents. namely Ij, C®, P?, M3. The cheek teeth were low-crowned and cuspi- date in the earliest family (Paramyidae) or higher crowned and crested in derived families (Ischyromyidae, Sciuravidae), but were always based on a pattern of no more than four transverse crests. Occa- sional Eocene forms plus most later ones had hypsodont or even ever-growing cheek teeth (Cylindrodontidae, Aplodontoidea). Locomotion was largely scampering (or arboreal scampering), though some deriva- tives of this group had developed burrow- ing locomotion (Cylindrodontidae, Myla- gualidae), and some may have been salta- torial (Protoptychidae). The angle of the lower jaw was essen- tially in the same vertical plane as the rest of the jaw, as is usual among mam- mals. Specifically, it is usually in the plane of the incisive alveolus (sciurogna- 471 RODENT GRADES 1 Fic. 1. Skull of the Eocene protrogomorph Jschyrotomus, with the jaw musculature restored, x 1. Abbreviations: M. LAT.—Masseter lateralis, dashed portions lying beneath Masseter superficialis ; M. PROF.—dashed lines indicating the course of the Masseter profundus; M. SUP.—Masseter super- ficialis; PT. E—dashed line indicating course of Pterygoideus externus; TEMP.—Temporalis. thous), though occasionally (Rezthropara- mys—W ood, 1962, fig. 41E) it has shifted to a position just laterad of the alveolus (incipiently hystricognathous). The chief components of the jaw mus- culature were the temporal, the pterygoid, and the masseter. All showed a certain amount of differentiation (Fig. 1). In a form such as /schyrotomus, the temporal was a large, fan-shaped muscle, arising in a semicircle from the frontal and parietal, and inserting on the coronoid process. Al- though the anterior fibers had a forward component and the posterior ones a back- ward component, its primary function was to raise the jaw, which pivoted about the condyle. The internal pterygoid, arising on the inner side of the pterygoid fossa and inserting on the inner surface of the angle (Wood, 1962, fig. 69B), pulled the jaw toward the midline as well as closing it. The external pterygoid (Fig. 1 PTE) arose on the external pterygoid process and inserted on the medial surface of the condyle. It helped to pull the jaw mesiad, but very largely served to slide the condyle forward and ventrad, along the glenoid cavity, to disengage the cheek teeth and bring the incisor tips into contact. The jaw was moved back again by the com- bined action of the temporal and the digas- tric. In /schyrotomus the areas of origin and insertion of the Masseter superficialis, M. lateralis, and M. medialis are readily sep- arable (Fig. 1). The Masseter medialis arose from the medial surface of the zy- goma and inserted on the dorsal surface of the masseteric fossa of the lower jaw. It pulled the jaw nearly straight upward. There was the beginning of a differentia- tion of this muscle into two portions, the anterior inserting on the masseteric tuberos- ity by a separate tendon. It seems prob- able that these parts were separated by the masseteric nerve. The Masseter later- alis arose from a fossa extending most of the length of the zygoma, and occupying the ventral third of the arch. It inserted over much of the lateral surface of the angle, and pulled the lower jaw laterally, upward, and slightly forward. The most superficial of the three divisions of the masseter was the Masseter superficialis, which arose from the masseteric fossa on the base of the maxillary portion of the zygoma, immediately laterad of the upper premolars, and inserted along the ventral margin of the jaw all the way to the angle. 472 118 ALBERT E. WOOD BiG 2s It was the major element in pulling the lower jaw forward, and hence in gnawing. The functional activity of the jaws was composed of three parts (Becht, 1953, p. 515). A vertical or transverse movement, with the condyle toward the posterior end of the glenoid cavity, was used in the chew- ing activities of the cheek teeth. This would have involved the use of the main part of the temporal, the two inner parts of the masseter, and the internal pterygoid, and is the usual mammalian chewing ac- tivity. If the condyle were moved forward to the anterior end of the sloping glenoid cavity, the cheek teeth would be disen- gaged, and the same combination of mus- cles plus the Masseter superficialis would provide the motion of the lower incisor against the upper, resulting in gnawing. The third component, the shift from the first position to the second, would be brought about by the anterior portion of the temporal, the external pterygoid, and the Messeter superficialis; the reverse by the posterior portion of the temporal and the digastric. The members of this grade include nearly all of the pre-Oligocene rodents of North America and Asia and some of those of Europe (none being known from the rest of the world). Several lines sur- vive into the Oligocene or early Miocene, and the Aplodontoidea occur from the Oligocene to the present, mostly in North Skull of the sciuromorphous sciurid Marmota, K 1. Abbreviations as for Fig. 1. America, although some aplodontids are present in Palaearctica. This grade seems to include forms so related that they may be considered to be a clade, the Suborder Protrogomorpha. GRADE Two—SECOND RADIATION Gnawing in the method outlined above was effective and presumably more effi- cient than that of the multituberculates or any of the other gnawing groups that were competing with the rodents in the Eocene. But the gradual filling of the available niches resulted in greater intra-ordinal competition and increased selective value for more efficient use of the incisors, which was brought about by a series of changes involving the muscles of mastica- tion, the skull structure, the incisors, and the cheek teeth. The modifications of the masseter mus- cle and the concomitant skull changes were the most prominent alterations lead- ing to Grade Two. These changes involved either the Masseter lateralis or the Mas- seter medialis or both, the Masseter super- ficialis remaining essentially unchanged. The Masseter lateralis may shift forward and upward, behind and median to the origin of the Masseter superficialis, onto the front of the zygomatic arch (Fig. 2). The shift was beginning in the ischyromy- ids Titanotheriomys (Wood, 1937, pp. 194-195, pl. 27, fig. 1, la, 1b) and Jschy- 473 RODENT GRADES 119 Fic. 3. Ventral part of M. profundus dotted. romys troxelli (op. cit., p. 191; Burt and Wood, 1960, p. 958), where the muscle was below, instead of lateral to, the infra- orbital foramen. This process continued, with the muscle origin moving forward and upward along the anterior face of the zygoma, passing lateral and dorsal to the infraorbital foramen, eventually reaching almost to the top of the snout and forward onto the premaxillary. This pattern char- acterizes the sciuromorphous rodents—the Sciuridae, Castoroidea, and Geomyoidea. This shift of origin has changed the direc- tion of pull of the anterior part of the Masseter lateralis by 30 to 60°, so that it essentially parallels the Masseter super- ficialis, greatly strengthening the forward component of masseteric action (Fig. 2). In other rodents, the anterior part of the Masseter medialis has spread from the inner surface of the zygoma (or, perhaps, from the medial margin of the orbit) for- ward through the enlarged infraorbital fora- men onto the snout (Fig. 3). In extreme cases, its origin extends as far forward as the premaxilla, almost reaching the pos- terior end of the external nares (Hydro- choerus, Pedetes, Thryonomys). This gives an almost horizontal resultant to the con- traction of this muscle, and strongly aug- Skull of the hystricomorphous caviomorph Myocastor, X 1. Abbreviations as for Fig. 1. ments the horizontal action of the Mas- seter superficialis. This pattern charac- terizes the hystricomorphous rodents—the Caviomorpha; the Dipodoidea, Theridom- yoidea, and Thryonomyoidea; and_ the Anomaluridae, Ctenodactylidae, Hystrici- dae, and Pedetidae. The Bathyergidae have developed per- haps the most massive masseters of any of the rodents, although there seems to have been very little shifting of the muscles (Tullberg, 1899, p. 78). The Masseter medialis has a broad expanse on the me- dian side of the orbit (perhaps associated with the reduction of the eyes) and is con- fluent with the anterior end of the Tem- poralis (Tullberg, op. cit., p. 75, and pl. 2, figs. 8-10, 17-18). In most members of the family, no part of the Masseter medi- alis passes through the small infraorbital foramen, but in Cryvptomys (= Georychus coecutiens, Tullberg, 1899, p. 79) a small portion just edges through the foramen (op. cit., pl. 2, fig. 17). Landry (1957, pp. 66-67) has argued that the small size of the infraorbital foramen and the limited forward extent of the Masseter medialis are secondary modifications of a hystrico- morphous pattern, and that. in spite of their differences, this family is relatively A474 Os eg 120 ALBERT E. WOOD SS M. PROF. Fic. 4. Skull of the myomorphous cricetid Ondatra, x 1.5. part of M. profundus dotted. closely related to the Hystricidae. Most authors would not accept this conclusion. Since the earliest known bathyergids, from the Miocene of Kenya, were essentially identical in masseteric structure to living forms (Lavocat, 1962, p. 292), it is im- possible to be certain of the direction of evolutionary change in this group. How- ever, the Masseter lateralis seems to be in the process of spreading forward and up- ward onto the anterior side of the snout. This, together with the enlarged expanse of the Masseter medialis on the mesial side of the orbit, seem to be jaw muscle migra- tions sufficient to place these forms in Grade Two. The expansion of the Masseter medialis onto the medial as well as lateral side of the orbit in bathyergids (Tullberg, 1899, pl. 2) and in Castor (op. cit., pl. 22, fig. 9), putting it in an ideal position to ex- pand through the infraorbital foramen if that opening were large enough, was prob- ably a structural antecedent of the hys- tricomorphous pattern. Whether or not it indicates any close relationship between these forms and any histricomorphous ro- dents is arguable. Finally, in the myomorphous rodents, both the Masseter lateralis and the Mas- Abbreviations as for Fig. 1. Ventral seter medialis have migrated, combining the features of the sciuromorphous and hystricomorphous groups (Fig. 4). This pattern characterizes the Muroidea, Spala- coidea, and Gliroidea. Such a type of mas- seter gives the greatest anteroposterior component of any of the types of rodent jaw musculature, with the possible excep- tion of the paca (Cuniculus). It is perhaps not a coincidence that this pattern is found in the Muroidea, the most successful and cosmopolitan of all rodents. At the same time that these changes in the masseter were occurring, the temporal muscle withdrew in most forms from the anterior area where it originated in /schy- rotomus, and is restricted in its origin to areas behind the tip of the coronoid proc- ess. In such forms it serves to raise the lower jaw and close the mouth or joins with the digastric and part of the Masseter medialis to move the jaw backward. How- ever, the temporal keeps its anterior area of origin in the Bathyergidae and in some of the Rhizomyidae. Whether the condi- tions in these two families are primitive or secondary is unknown. The reduction of the temporal muscle continued in many rodents, especially those with enlarged auditory bullae (Howell, 1932, p. 411), so 475 RODENT GRADES that in some it eventually became reduced to an exceedingly minute slip (Tullberg, 1899, pl. 9, figs. 8-9, Ctenodactylus; pl. 10, figs. 8-9, Pedetes; pl. 12, Dipus and Alactaga; and pl. 23, figs. 18-20, Dipod- omys). All of the sciuromorphous and myo- morphous rodents and a number of the hystricomorphous ones (Theridomyoidea, Anomaluridae, Ctenodactylidae, and Pede- tidae) have an angular process of the sciurognathous type, with the angle in the plane of the incisive alveolus. This is un- doubtedly the primitive condition. In the other hystricomorphous rodents, the angle has shifted until it arises quite markedly laterad of the incisor. This would make the Masseter lateralis and M. superficialis more nearly vertical. This hystricogna- thous arrangement is fully developed in the earliest known (early Oligocene) members of the South American subordinal clade Caviomorpha (Wood and Patterson, 1959, p. 289) and of the African clade Thryono- myoidea (Wood, Ms. 1), as well as in the Hystricidae, apparently of south Asiatic origin (Lavocat, 1962, pp. 292-293), and in the Bathyergidae. Associated with these changes in the jaw muscles, but not necessarily occurring at precisely the same time, nor necessarily functionally correlated, there have been changes in the incisors, involving both their angulation and their histology. The lower incisors have usually become arcs of larger circles, so that they are more nearly hori- zontal, with the tips moving anteroposte- riorly against the upper incisors. The upper incisors have tended to become either larger or smaller arcs, so that the tips tend to point either forward (true usually of burrowing forms), or slightly backward as is true of most living rodents. The former of these adjustments increases the ability to use the incisors as digging implements, with a corresponding increase in the rate of growth of the incisors, which reaches almost 0.5 cm per week in the lower in- cisors of geomyids (Manaro, 1959). The second change brings the enamel blades of 121 the upper and lower incisors more nearly into direct opposition than was true in Grade One. Changes also took place in the histology of the incisor enamel. The pauciserial type has been modified, in members of Grade Two, in two different directions. In the uniserial type (Korvenkontio, 1934, p. 227), the lamellae are regular, and made up of one row of prisms each, with the prisms oriented in opposite directions in successive lamellae. This pattern is found in the Sciuridae, Castoridae, Geomyoidea, Gliridae, Muroidea, Spalacidae, Dipodoid- ea, and Anomaluridae among members of Grade Two, and in Aplodontia, Menisco- mys, and Ischyromys among the members of Grade One (Korvenkotio, 1934, table on pp. 116-123). The situation among the Theridomy- oidea is most instructive. In the middle Eocene to Oligocene Pseudosciuridae, which are fully hystricomorphous in the infraorbital structure, the incisors are still pauciserial. The same is true of the more primitive members of the Theridomyidae, such as Theridomys. In more advanced theridomyids, there is a complete transi- tion to the uniserial type of enamel. In Issiodoromys |= Nesokerodon| minor, Korvenkontio describes the enamel as “pauci-uniserial” (op. cit., p. 116). He further describes that of Protechimys gra- cilis as pauciserial, and that of Archaeoniys laurillardi as uniserial. These two forms are currently recognized as being two spe- cies of Archaeomys (Schaub, 1958, figs. 48-49). So in the Theridomyoidea, the transition from Grade One to Grade Two has occurred later in the incisor enamel than it did in the jaw musculature, the two apparently being completely independent. A different type of enamel modification occurs in what Korvenkontio (op. cit., p. 130) calls the multiserial type. Here each lamella is formed of four to seven identi- cally oriented rows of prisms, the lamellae lying at an angle of about 45° to the sur- face of the enamel. Successive lamellae have the prisms oriented in opposite direc- 476 122 tions (Korvenkontio, 1934, pl. 8, figs. 3, 5, 7). This occurs in the Caviomorpha, and the Bathyergidae, Ctenodactylidae, Hystricidae, and Pedetidae. Finally, there are likely to be differences in cheek-tooth formula or pattern associ- ated with the change to Grade Two from Grade One. Primitively, the rodent cheek- tooth formula was P? and M3, although some members of Grade One have lost P°. This tooth has been preserved today only in A plodontia and among the Sciuridae. In many rodents (most Caviomorpha, Anom- aluridae, Castoroidea, Ctenodactylidae, Geomyoidea, Gliroidea, Hystricidae, and probably Pedetidae), P{ have been re- tained. In such caviomorphs as_ the Echimyidae (Friant, 1936) and Capromy- idae (Wood and Patterson, 1959, p. 324) and in the living African Thryonomyoidea (Wood, 1962, p. 316-317), the permanent premolars have been suppressed and the deciduous premolars are retained through- out life. This may also be true for the Pedetidae (Wood, ms. 2). According to Schaub (1958, p. 678), the reverse of this process occurs, with the elimination of the deciduous tooth in many hystricomorphous forms. Finally, the Muroidea and Spalacoi- dea have lost all the premolars and the Dipodoidea have almost reached this stage. In summary, in Grade Two, there is a tendency to reduce the length of the tooth row, probably an adaptation permitting greater contrast between the gnawing and chewing activities, and therefore greater specialization in each. Usually, the loss of these teeth occurred at times when there are still gaps in the paleontological history of the groups. However, the loss of P? oc- curs within the known history of the Eomyidae (Wood, 1955b) and Gliridae (Schaub, 1958, figs. 201, 203), and the presence of P* is variable in living mem- bers of the Dipodidae (Schaub, 1958, p. 792). Although the loss of cheek teeth brought about greater specialization of gnawing and chewing activities, it may have interfered with the functional activities of chewing, ALBERT E. WOOD since in almost all members of Grade Two there has been a tendency secondarily to elongate the cheek teeth by developing an additional transverse crest (mesoloph or mesolophid) in the middle of the teeth, making them five-crested in contrast to the four-crested pattern found in Grade One. This five-crested stage seems cer- tainly to have developed independently in many lines, and therefore is no better than any other single criterion in determining the phylogenetic relationships (clades) among the rodents. The changes in the jaw musculature look as though they are indicative of genetic re- lationships (i.e., clades), and were so used by most authors as far back as Brandt (1855) or even earlier, until fairly recent- ly, giving three suborders of rodents, the Sciuromorpha, Hystricomorpha, and Myo- morpha (see Simpson, 1945). However, the use of other criteria for rodent classification complicated this ap- parently simple pattern. Tullberg (1899), for example, showed that rodents could be divided into two groups on the basis of the way in which the angle of the lower jaw originated—the Sciuragnathi, in which the angle arises in the plane of the alveolus of the lower incisor, and the Hystricogna- thi, in which it arises lateral to this plane. The hystricognathous forms include only those that are more or less hystricomor- phous, whereas the sciurognathous ones may be sciuromorphous, myomorphous or hystricomorphous. With an increase in the detailed studies of rodent paleontology since 1920, the chance that any of the three Brandtian suborders represents a clade has become progressively smaller, and students of fossil rodents have universally abandoned them at present. The Sciuromorpha may be considered to be typical. The sciuromorphous condi- tion was achieved by the squirrels (Sciur- idae) in a transition, which is as yet not completely documented but that seems very probable, from a mid-Eocene para- myid such as Uriscus (Wood, 1962, p. 247; A477 RODENT GRADES Black, 1963, p. 229). A similar trend, not carried so far, is seen in the Oligocene ischyromyids, Titanotheriomys (Wood, 1937, pp. 194-195) and some species of Ischyromys (Burt and Wood, 1960, p. 958). These forms could not be in the ancestry of the squirrels, as their cheek- tooth pattern is much more advanced than is that of the squirrels. The sciuromorphous Geomyoidea (in- cluding the extinct Eomyidae as well as the Geomyidae and Heteromyidae) seem to have many fundamental similarities espe- cially in the basicranium (Wilson, 1949, pp. 42-48; Galbreath, 1961, pp. 226-230), to the myomorphous Muroidea (Muridae, Cricetidae), and have probably come from a common source. Whether this source was a sciuromorphous form, among some of whose descendants the Masseter medialis shifted forward, or whether it was a pro- trogomorphous form, and one group of descendants shifted the Masseter lateralis alone and the other shifted both branches of the muscle simultaneously, is completely unknown. It seems rather probable, how- ever, that the Geomyoidea and the Muro- idea are descended from some member of Grade One that would be included among the Sciuravidae. The jaw mechanism of the beavers (Castoridae) and their Oligo- cene to Miocene relatives, the Eutypomy- idae, is almost identical to that of the squirrels, except for the expansion of the Masseter medialis onto the median side of the orbit. At present there is no evidence as to the pre-beaver ancestry of this group. The tooth structure of the Castoroidea is completely different from that of any of the other sciuromorphous rodents, which has led Schaub to include them, with the Theridomyoidea and Hystricoidea, in his Infraorder Palaeotrogomorpha (1958, p. 694). This association seems unnatural. It is possible that there is a special rela- tionship of the beavers with either the ischyromyids or the sciurids, although the presence of five-crested teeth in both upper and lower jaws of the beavers makes this seem very unlikely. 123 The evidence that masseteric structure represents a grade is equally clear among the hystricomorphous rodents. These in- clude the Old World porcupines (Hystri- cidae); the African Oligocene to Recent Thryonomyoidea (Cane Rats, Rock Rats, and Phiomyidae); the isolated African families Anomaluridae, Bathyergidae, Cten- odactylidae, and Pedetidae; the European Eocene to Oligocene Theridomyoidea; the South American Caviomorpha; and, as al- ready indicated, the Dipodoidea. The lines of descent of most of these groups are either not clear or are unknown. The South American forms are a natural unit, the Suborder Caviomorpha of Wood and Pat- terson (1959, p. 289) or the Infraorder Nototrogomorpha of Schaub (1958, p. 720). It seems certain that these rodents have evolved in isolation in South America since the late Eocene or early Oligocene, when at least some members of the group were fully hystricomorphous and all were hystricognathous, and that they have had no connections with any other hystrico- morphous forms during that period. On the basis of the available evidence, the most reasonable explanation for them is that they represent derivatives of a North American Grade One stock, that managed to reach South America by island hopping during the late Eocene, either via Middle America (Simpson, 1950, p. 375; Wood, 1962, p. 248; Wood and Patterson, 1959, p. 401-406), or via the West Indies (Lan- dry, 1957, p. 91, who believed that these were hystricomorphs from the Old World; Wood, 1949, p. 47). The African Thryon- omyoidea are clearly derived from the Oligocene to Miocene Phiomyidae (Lavo- cat, 1962, p. 289), whose Oligocene mem- bers (Wood, ms. 1) show no signs of rela- tionship with any other group of hystrico- morphous rodents, and can only (at pres- ent) be considered as an independent line derived from unknown _ protrogomorphs. The Hystricidae (all that seems to be left of the old Hystricomorpha) seem to have had a south Asiatic origin and differentia- tion, whence they spread, in the late Mio- 478 124 cene or early Pliocene, to Europe and Africa. The Bathyergoidea are, unfortu- nately, very poorly known as_ fossils, though they occur in the African Miocene (Lavocat, 1962, p. 290). Certain Mon- golian Oligocene fossils that have some- times been referred to this family (Mat- thew and Granger, 1923, p. 2-5; Landry, 1957, pp. 72-73) have generally been agreed probably to be late members of the Grade One Cylindrodontidae. The other hystricomorphous groups are all sciurognathous. The Dipodoidea (Dip- odidae, Zapodidae) are extremely close to the cricetids in tooth pattern—so close, in fact, that many Miocene and Pliocene zapodids were originally referred to the Cricetidae (Schaub, 1930, pp. 616-617, 627-629; Wood, 1935b, Schaubeumys; Hall, 1930, Macrognathomys). The skel- etal and myological differences between the Muroidea and Dipodoidea also seem to be relatively minor, and the Dipodoidea almost certainly belong to the same clade as do the Muroidea and Geomyoidea, which may be called the suborder Myo- morpha. The Theridomyoidea are an Eocene— Oligocene group, not known outside of Europe. The earliest members of the super- family are close to the Paramyidae in cheek-tooth structure (Wood, 1962, p. 170) and in enamel histology (Korven- kontio, 1934, pp. 96-97), but are already fully hystricomorphous. It was long cus- tomary to consider them ancestral to the Caviomorpha, with the descendants, among other things, becoming hystricognathous. This interpretation is easily read into Schaub’s classification, although he spe- cifically states that current knowledge is not adequate to demonstrate such a rela- tionship (1958, p. 693). But the closest resemblances to the theridomyoid tooth pattern are mot found in the earliest cavio- morphs as should be the case if they were genetically related (Wood and Patterson, 1959, pp. 400-401). Current work makes it equally improbable that there is a theridomyoid-thryonomyoid _ relationship ALBERT E. WOOD (Wood, Ms. 1). The earliest known Anom- aluridae are from the Miocene of Africa. There is no good evidence indicating rela- tionship between them and any other group of rodents. It is conceivable that they are related to the Theridomyoidea, but there is no real evidence for such a relationship. The Ctenodactylidae, now exclusively Af- rican, have been shown by Bohlin (1946, pp. 75-146) to be abundant in the Oligo- cene of central Asia, and are known from Africa only since the late Miocene (Lavo- cat, 1962, p. 289). Work in _ progress (Dawson, 1964) rather strongly suggests an independent derivation of this family within central Asia from members of Grade One, though the jaw muscle transitions have not been worked out. Finally, the Pedetidae are in many ways the most isolated of all rodents. They have lived in Africa since the Miocene (Stromer, 1926, pp. 128-134; MaclInnes, 1957), and have a tooth pattern which is only very slightly reminiscent of that of any other rodents. They probably (with no evidence) represent an independent derivation from members of Grade One (Wood, Ms. 2). Schaub (various. sources, especially 1958) completely abandoned the use of the zygomasseteric structure or that of the angle, in the subordinal classification of rodents, and relied only on the cheek- tooth pattern. He argued extensively (1958, p. 684, 691-694) that either the five-crested pattern (“plan Theridomys’’) originated only once, in the Theridomyo- idea, and that all other five-crested forms are descended from them, or that his sub- order Pentalophodonta, including these forms, is a natural group (clade) in that it contains those forms, and only those forms, that have achieved a five-crested pattern as a result of parallelism. As he stated (op. cit., p. 693), our current knowl- edge of the detailed phylogeny of the ro- dents is still inadequate to permit us to make positive statements of the exact an- cestry of most of the families of what are here included in Grade Two. Schaub fur- 479 RODENT GRADES ther stated: “Il me parait aussi évident que Vidée de ce plan fondamental qui nous permet de révéler sinon tous, mais presque tous les parallélismes, peut servir comme base utilisable de la classification, tandis qu’on ne peut pas placer la méme confiance dans celles qui s’appuie sur les structures zygo-massétériques et la configuration de langle mandibulaire” (op. cit., p. 693). The current conclusion of most students of fossil rodents is that there is no simple key to separating clades from grades within this complex order, and that no one set of criteria (tooth patterns, zygomasseteric structure, type of angle, fusion of ear ossicles, incisor histology, etc.) may be re- lied upon. Parallelisms and convergences are so abundant that only an analysis of all possible criteria can give reliable evi- dences of cladal unity (Lavocat, 1962, p. 288). From the analysis of the features that are used to separate members of Grade Two from those of Grade One (jaw mus- culature; angle of the jaw; incisor posi- tion; incisor histology; cheek-tooth for- mula and pattern), it seems quite clear that these features evolved independently of each other. Hystricomorphous forms can be either hystricognathous or sciur- ognathous; any clade of Grade Two can include forms with high-crowned, as well as low-crowned, cheek teeth; and the changes in incisor histology seem to have taken place independently of all the others. This situation is not surprising and should not cause insurmountable difficulties in classification. It merely emphasizes that the grades must not be interpreted as clades, and that a key, based on grade characters, may be useful but is still only a key. GRADE THREE—HYPSODONTY AND PATTERN MODIFICATION The third grade in rodent evolution is not as clear-cut as are the first two. It is represented by those members of Grades One or Two that have developed extremely hypsodont or ever-growing cheek teeth. 125 These have developed independently many times, in almost all clades of rodents, as adaptations to grazing or burrowing modes of living. Among protrogomorphs, the bur- rowing cylindrodonts, the perhaps steppe- living protoptychids, the aplodontids and the mylagaulids all become very hypso- dont. There is a definite trend toward hypsodonty in burrowing squirrels (Cyno- mys) and in some of the Old World ground squirrels. The burrowing geomyids and the desert-living saltatorial heteromyids have ever-growing cheek teeth. Extremely high crowns also characterize most of the Caviomorpha except for the New World porcupines (Erethizontidae) ; the Thryono- myoidea, the Bathyergidae, Ctenodactyli- dae, and Pedetidae in Africa; the Spalaci- dae and Rhizomyidae; the Castoridae; and the Microtinae among the Cricetidae. Perhaps the suppression of the premolars and retention of the deciduous teeth, dis- cussed above, are also features of this grade. On theoretical grounds, it would seem that a good explanation might be that the wear of the cheek teeth was so rapid that selection for increase of height of dP{ was very strong, resulting in teeth that would last, proportionately, as long as in low-crowned ancestral forms. A long-growing tooth of this sort would be capable of increasing its horizontal dimen- sions, thus eliminating the primary adap- tive reason for the replacement of decidu- ous teeth by permanent ones—the fact that the baby jaws were not big enough for adult-sized teeth. However, in the only case where the details of the suppres- sion of P# by retained dP{ are known (Phiomyidae, Wood, ms. 1), this change is taking place in animals some of which are still low-crowned while others are, at most, mesodont. Two types of ever-growing teeth have developed among rodents. Usually, there has been growth of the pattern-bearing portion of the crown, so that the pattern is preserved with wear—at least in consider- able part. This has resulted in cheek teeth that lose the details of cusp arrangement 480 126 early in life, but in which a characteristic pattern is quickly achieved, and retained for the rest of the animal’s lifetime. Such patterns are found in most caviomorphs, the Thryonomyoidea, the Theridomyidae, Bathyergidae, Ctenodactylidae, Pedetidae, Rhizomyidae, Castoridae, Spalacidae, and Microtinae. In some rodents, however, there is little or no growth of the pattern-bearing portion of the crown, but rather a strong unilateral hypsodonty of the basal part of the crown. This arrangement usually results in the re- duction of the enamel to one or a few trans- verse plates on each tooth, alternating with dentine (or occasionally cement) prisms. Such pattern developments are most char- acteristically developed in the Geomyidae (Merriam, 1895; Wood, 1936) and Heter- omyidae (Wood, 1935a). Similar develop- ments are present in Mongolian Oligocene cylindrodonts (Schaub, 1958, fig. 156), in several cases among caviomorphs (Wood and Patterson, 1959, p. 333 et seq.; figs. 9A, 14C, 16B, 23A), and in advanced the- ridomyids (Schaub, 1958, figs. 45, 49, 51, and 50). The tendency to elongate the cheek teeth, discussed above under Grade Two, has been continued in a considerable num- ber of forms by developments at the front end of the anterior cheek teeth (the antero- cone and anteroconid), or by additions at the rear of the last tooth. The former is especially characteristic of the Microtinae, the latter of the Hydrochoeridae. There can be no possible doubt that these high-crowned or ever-growing cheek teeth have been acquired independently in the various clades that are involved. GRADE ZERO—THE Basic LEVEL The evidence suggests that the Paleocene rodent differentiation was based on a dis- tinctly more primitive level of gnawing ability than that seen in later forms. This radiation, while essentially hypothetical, can be fairly well characterized, and is here called Grade Zero. Among middle Eocene and later rodents, ALBERT E. WOOD the incisors universally have an enamel cap that covers the entire front face, and that curves around onto the buccal and lingual sides of the tooth for a short dis- tance, serving to lock the enamel firmly onto the dentine. Among some of the ear- liest rodents of the Family Paramyidae, however, the locked-on pattern of enamel had not been achieved and the enamel merely forms a strip extending across most (but not all) of the width of the front edge of the tooth. As a result, there would have been danger of chipping or breaking off pieces of the enamel strip. This pat- tern shows up well in the late Paleocene Paramys atavus (Wood, 1962, fig. 21 B, C), and is also suggested in many individ- ual specimens of several early Eocene paramyids, which seem to represent the last remnants of this Paleocene radiation. The early development of the Leptotomus incisor pattern, with the enamel extending over a very large part of the tooth, may also be derived from such a basic condi- tion. While there is no evidence one way or the other, it would seem entirely possible that the rodents of Grade Zero had a com- plete enamel cap on the unworn incisors, as did the multituberculates, and had merely achieved extreme unilateral hypso- donty. At some unknown time during the Paleocene, the rodents achieved a level where the incisors, including the enamel strip, became ever growing. Since the few known late Paleocene rodent incisors are all fragments, it cannot be determined when this condition was reached, though these incisor fragments seem to belong to ever-growing teeth similar (in this respect) to those of Grade One. This suggests that this type of tooth began to be acquired not later than middle Paleocene. In the early rodents or their immediate precursors there was a reduction from the primitive placental formula of I} Cj} P} M: to that characteristic of the early Eocene Paramyidae, I} C!) P? M3. This almost cer- tainly had taken place well before the end of the Paleocene, and presumably had be- 48] RODENT GRADES gun before the enlargement of the incisors was completed. The difference between the jaw mus- culature of Grade One (Fig. 1) and that of primitive mammals was presumably not very great, if Edgeworth’s figures (1935, fig. 692a, b, p. 459) of the musculature of Dasyurus are any criterion. Here the Mas- seter superficialis has the same anteropos- terior alignment as in /schyrotomus, and the Masseter lateralis and Masseter medi- alis (Masseter profundus and Zygomatico- mandibularis of Edgeworth) have an al- most vertical alignment. Thus, the Dasyu- rus pattern of jaw musculature seems pre- adaptive for the beginnings of gnawing ro- dents, and therefore probably is essentially what was found in Grade Zero. The skull structure of Paleocene rodents is completely unknown. But it seems prob- able that the development of free antero- posterior movement of the condyle of the lower jaw occurred pari passu with the de- velopment of extremely hypsodont to ever-growing incisors and the reduction of the dental formula discussed above, and that the structure of the condyle and glenoid fossa, of the incisors, of the cheek teeth and of the jaw muscles evolved as a unit complex. DISCUSSION The analysis of rodent morphological evolution, given above, involves the inter- pretation of the classical suborders, the Sciuromorpha, Myomorpha, and Hystrico- morpha, as representing alternative expres- sions of a major and a secondary adaptive level in the order, here called Grade Two and Grade Three. In all cases, they seem clearly not to be clades. The Protrogo- morpha, as defined by Wood (1959, p. 170) are a closer approach to being both a clade and a grade. This suborder does not quite coincide with a grade because some members, while not having achieved any of the specializations of Grade Two, have reached a level of dental complexity that is here considered indicative of Grade Three. Whether the Protrogomorpha, as 127 here delimited, can be considered to rep- resent a clade, is perhaps arguable. Cer- tainly the Ischyromyoidea are a clade. Certainly the Aplodontoidea are derived from them, but most authors consider that the same is true of all the other rodents as well. However, the Protrogomorpha, as here defined, are related forms that have structural features in common, permitting the group to be satisfactorily defined. Black has recently (1963, pp. 126-128) argued that the Sciuridae, because of their primitive dentition, should be returned to the Protrogomorpha, where Wood once in- cluded them (1955a). The suborder could then be defined as members of Grade One plus certain groups that had not gone very far in evolving into Grades Two or Three. It seems better, however, for the present to use the break between Grade One and Grade Two as a fundamental division in rodent classification, and hence to elim- inate the Sciuridae from the Protrogo- morpha. A major reason why Black con- siders that the squirrels can no longer be separated from the members of Grade One is that Miosciurus and Protosciurus, from the early Miocene, have zygomasseteric structures that have not fully achieved the sciuromorphous pattern. However, his de- scription (1963, pp. 136, 140) and figures (op. cit., pls. 3, 6) show that the masseter had already begun its migration in these forms, so that, technically, they belong to what is here called Grade Two. Naturally, there had to have been a transition from Grade One to Grade Two, and the transi- tional forms would be hard to place with exactitude, but it seems best to consider all the known Sciuridae as members of Grade Two. The rest of the cladal classification of rodents must still remain largely as in- dicated by Simpson (1959) and Wood (1959, p. 172). The main changes that are required at the present time involve certain African rodents. The Phiomyidae are clearly not Protrogomorpha, but are hystricomorphous forms ancestral to the Thryonomyoidea, to which superfamily 482 128 they should be referred. There seems to be even less justification than formerly (Wood, 1955a) for placing the Hystricidae close to any other known families. All the available evidence suggests that the level of Grade Two has been achieved many times independently. Instead of the three suborders that were formerly rec- ognized, it seems better to recognize at least eleven clades that have independently passed from Grade One to Grade Two. Which of these should be considered sub- orders and which merely families or super- families is, for the moment, largely a mat- ter of convenience (Simpson, 1959; Wood, 1959). A cladal classification of rodents, based on current knowledge, is as follows: Order Rodentia Suborder Protrogomorpha Superfamily Ischyromyoidea Paramyidae, Sciuravidae, Cylindrodonti- dae, Protoptychidae, and Ischyromyidae Superfamily Aplodontoidea Mylagaulidae and Aplodontidae Suborder Caviomorpha Superfamily Octodontoidea Octodontidae, Echimyidae, Ctenomyidae, Abrocomidae, and Capromyidae Superfamily Chinchilloidea Chinchillidae, Dasyproctidae (incl. Ce- phalomyidae), Cuniculidae, Heptaxodon- tidae, and Dinomyidae Superfamily Cavioidea Eocardiidae, Caviidae, and Hydrochoeri- dae Superfamily Erethizontoidea Erethizontidae Suborder Myomorpha Superfamily Muroidea Cricetidae (incl. Melissiodontidae Schaub) and Muridae (incl. Gerbillidae Stehlin and Schaub) Superfamily Geomyoidea Geomyidae, Heteromyidae, and Eomyi- dae Superfamily Dipodoidea Dipodidae and Zapodidae Superfamily Spalacoidea Spalacidae and Rhizomyidae Superfamily Gliroidea Gliridae and Seleveniidae Clades not in suborders: Family Sciuridae (incl. Eupetauridae Schaub and Iomyidae Schaub) Superfamily Castoroidea ALBERT E. WOOD Castoridae and Eutypomyidae Superfamily Theridomyoidea Pseudosciuridae and Theridomyidae Family Ctenodactylidae (incl. Tataromyidae Bohlin) Family Anomaluridae Family Pedetidae Family Hystricidae Superfamily Thryonomyoidea Phiomyidae (incl. Diamantomyidae Schaub), Thryonomyidae, and Petromuridae Family Bathyergidae The Family Pellegriniidae of Schaub is based on a single species of completely un- known affinities, which should not be con- sidered a family until more is known about te SUMMARY Rodent evolution can be envisioned as involving three relatively clear-cut evolu- tionary levels, here called Grades One, Two, and Three. The first involves well- developed gnawing animals, with a primi- tive mammalian jaw musculature. Grade Two includes those animals that have mod- ified the jaw musculature in one of sev- eral ways that formerly were used as the basis for rodent subordinal classification. There were also changes in the dentition, especially in the development of cheek teeth with five transverse crests, rather than ones with no more than four crests as in Grade One. Changes occurred in nu- merous other parts of the skeleton and dentition, although these were probably not correlated with each other. Grade Three includes those rodents with very high-crowned or even ever-growing cheek teeth, in which there is sometimes the same type of limitation of the enamel that oc- curred during the Paleocene on the in- cisors. Grade Three also includes forms in which there has been a marked second- ary increase in the length of the cheek teeth. A hypothetical Grade Zero is imag- ined for the rodents of the second half of the Paleocene. Only Grade One comes close to approxi- mating a clade. The Protrogomorpha, as here defined, include the members of Grade One and some forms that have 483 RODENT GRADES reached Grade Three without going through Grade Two. The cladal classification of the rodents still requires the recognition of numerous independent lines, showing no evidence of interrelationship later than in members of Grade One. Only two or pos- sibly three clades can be recognized that require units larger than the superfamily— the Protrogomorpha, the Caviomorpha, and perhaps the Myomorpha. The other ro- dents fall into nine familial or superfamilial clades. ACKNOWLEDGMENTS A discussion of the similarities and dif- ferences between rodent and teleost evolu- tion prompted Schaeffer to make the oral suggestion that an analysis of evolutionary grades and clades among rodents would be very useful to students of the evolution of other groups. This has led to the prepara- tion of the present review. This study was assisted by grants from the National Sci- ence Foundation and from the Marsh Fund of the National Academy of Sciences. LITERATURE CITED Becut, G. 1953. Comparative biologic-anatom- ical researches on mastication in some mam- mals. Konink. Nederl. Akad. Wetensch., Proc., C, 56: 508-527. Brack, C. C. 1963. A review of the North American Tertiary Sciuridae. Bull. Mus. Comp. Zool., 130: 109-248. Boutin, B. 1946. The fossil mammals from the Tertiary deposit of Taben-buluk, Western Kansu. Part II. Simplicidentata, Carnivora, Artiodactyla, Perissodactyla, and Primates. Rept. Scientific Exped. North-western Prov. China under leadership of Dr. Sven Hedin, 6, Vertebrate Paleontology, no. 4: 1-259. BranptT, J. F. 1855. Beitrage zur nahern Kennt- niss der Saugethiere Russlands. Mém. Acad. Imp. Sci. St.-Pétersbourg, ser. 6, 9: 1-375. Burt, A. M., ano A. E. Woop. 1960. Variants among Middle Oligocene rodents and lago- morphs. J. Paleont., 34: 957-960. Dawson, M. 1964. Late Eocene rodents (Mam- malia) from Inner Mongolia. Amer. Mus. Novitates, 2191: 1-15. EpGreworTtH, F. H. 1935. The cranial muscles of vertebrates. Cambridge Univ. Press. ix + 493 pp. Friant, M. 1936. Interprétation des dents jug- ales chez les lonchérinés. Vidensk. Med. Dansk. nat. For. Kjgbenhavn, 99: 263-266. 129 GALBREATH, E. C. 1961. The skull of Helisco- mys, an Oligocene heteromyid rodent. Trans. Kansas Acad. Sci., 64: 225-230. Hart, E. R. 1930. Rodents and lagomorphs from the later Tertiary of Fish Lake Valley, Nevada. Univ. California Publ. Geol., 19: 295-312. Howe tt, A. B. 1932. The saltatorial rodent Dipodomys: the functional and comparative anatomy of its muscular and osseous systems. Proc. Amer. Acad. Arts and Sci., 67: 377- 536. Huxtey, J. S. 1958. Evolutionary processes and taxonomy with special reference to grades. Uppsala Univ. Arssks., 1958: 21-38. KorvenkonTio, V. %e River SS Se ois) —- = nevadensis asin eg on 34 ! SEE Le | UTAH g ee j Fic. 3—Map of Montana-Wyoming-Idaho border area, showing partial ranges of taxa discussed, and certain physiographic features of the region. Open spots indicate localities for Spermophilus r. richard- sonii; solid spots indicate localities for S. r. aureus. to be only 20-25 miles long. It is restricted to the lower Madison River valley (Figs. 1, 3) by barriers of unsuitable montane habi- tat; the Yellowstone Plateau complex to the south and east, of which the Madison and Gallatin Ranges comprise the north- west comer; and the Tobacco Root and Elk- hom Mountains to the north, cut through by the precipitous Jefferson River Canyon (Fig. 3). Ground squirrels of the S. rich- ardsonii complex inhabit valley bottoms and foothills in southwestern Montana and adjacent Idaho (Durrant and Hansen, 1954), and not mountain meadows, as S. r. elegans does in Colorado (Hansen, 1962; Lechleitner, 1969). Mountain meadows in the Montana-Wyoming-Idaho border area are instead inhabited by S. armatus, a ground squirrel similar to S. r. aureus and S. r. elegans both morphologically (Davis, 1939), and cytologically (Nadler, 1966). The montane barriers to S. richardsonii may thus contain both habitat and biotic (com- petitive) components (Durrant and Hansen, 1954; Hoffmann, et al., 1969). Only one of 21 colonies studied con- tained identifiable (2n = 35) hybrids, and within this colony the hybrid frequency, in 1969, was only 4/24. The narrowness of the zone of potential contact and infre- quency of hybrids suggests that the situa- tion is not now one of chromosomal polymorphism, wherein more than one karyotype is found within a single, po- tentially panmictic population, such as has been described for certain rodents ( Matt- hey, 1963a, b). There is evidence that aureus and richardsonii ground squirrels 489 302 have occupied the general area for at least a century (Merriam, 1891) and the contact zone for over 50 years; specimens of both taxa collected in 1917-18 are in the collec- tion of the Department of Zoology and Entomology, Montana State University, Bozeman. They may, of course, have ex- isted here much longer. Despite the long period of contact, and the considerable dispersal powers of ground squirrels (Han- sen, 1962), hybridization is rare. This sug- gests either that behavioral or other barriers are inhibiting hybridization, or that some sort of selection is acting against the hy- brids relative to the parental types. Hybrid fertility has not yet been tested, but one adult female hybrid collected was lactating, evidence that a fertility barrier to gene exchange may not be complete. The isolated ranges of the three pheneti- cally similar 2n = 34 taxa (nevadensis, elegans, aureus) (Fig. 3) suggests that the present distributional disjunctions have re- sulted from fragmentation of a formerly continuous range across the Snake River Plain of southern Idaho. The present-day absence of this ground squirrel on the Snake River Plain may be due to post-glacial changes in the physical environment and/or displacement by S. townsendii. Such a dis- tribution pattern, centering on the northern Great Basin and adjacent desert plateaus and basins, contrasts with the present-day continuous distribution of S. r. richardsonii (2n = 36) on the northern Great Plains. The distributional patterns of a number of species of mammals suggests that the Great Basin and Great Plains were two important centers of differentiation during the Pleisto- cene (Hoffmann and Jones, 1970). The question of which ground squirrel taxon is closer to the ancestral population cannot be answered unequivocally. The disjunct, relict distribution of the 2n = 34 ground squirrels argues for their being the older group (Hoffmann and Jones, 1970). Moreover, the oldest known fossil of the richardsonii complex is assigned to S. r. elegans (2n = 34); it occurs in sediments deposited during the Kansan glacial period SYSTEMATIC ZOOLOGY (Hibbard, 1937). Much of the area pres- ently occupied by S. r. richardsonii was either covered by glacial ice, or supported a boreal coniferous forest during the last glacial period, the Wisconsin (Lemke, et al., 1965; Wells, 1970). These factors must have restricted suitable ground squirrel habitat within the present range of S. r. richardsonii to a relatively small area from central Montana perhaps to western North Dakota. To the north was the ice sheet, to the east, coniferous forest, and to the west, the forested mountains of the Continental Divide. There are, remarkably, no S. r. richard- sonii at present known from south of the Yellowstone River in Montana or south and west of the Missouri River in North and South Dakota. There is thus a large area of apparently suitable habitat in the un- glaciated area of southeastern Montana, southwestern North Dakota, northeastern Wyoming, and western South Dakota where the species does not occur; neither are there closely-related species which might serve as ecological equivalents. The Yellow- stone-Missouri system thus seems to limit the distribution of S. r. richardsonii along the southern edge of its range. However, the upper Yellowstone has only recently become a major river due to late-Wisconsin capture of the drainage of the Yellowstone Plateau, much of which had _ formerly drained westward into the Snake River. Prior to that event, the main tributaries of the Yellowstone were the Bighorn and Powder rivers, and above the Bighorn the Yellowstone was probably quite small (Fenneman, 1931; Lemke et al., 1965). All of these data suggest that S. r. rich- ardsonii has occupied its present range on the northern Great Plains as the glacial ice and coniferous forests retreated in post- glacial time, and that it spread from an area of origin north and west of the Yellow- stone River after the Yellowstone River achieved its present size. Two models could account for such an origin and spread. The first involves split- ting, one or more times, of an ancestral 490 GROUND SQUIRREL CHROMOSOMAL DIVERGENCE 303 population into separate units by forested barriers that developed in a glacial period (Wisconsin or earlier). During glacial periods, a barrier of continuous boreo- montane forest (Findley and Anderson, 1956) evidently separated the Great Basin and the Snake River Plain from the northern Great Plains (Fig. 3). If the ancestral form of the richardsonii complex were separated into two or more populations isolated on either side of this barrier, these might dif- ferentiate, undergo chromosomal changes and eventually develop a partially effective isolating mechanism. The population on the northern Great Plains was subjected to extreme conditions during glacial maxima, during which its range was sharply con- stricted. Such a population, subjected to “catastrophic selection,” might be induced through forced inbreeding into chromo- somal reorganization, as Lewis (1966) de- scribes. Such a “founder” population (Mayr, 1963) would then have the opportunity to spread rapidly into the large area of the northern Great Plains made available by post-glacial retreat of the ice sheets. At the same time, during inter- or post-glacial periods, when non-forested connections were re-established between the Snake River Plain and the northem Great Plains, ground squirrels could then spread over low passes and come into contact again. The second alternative is that the “founder” population arose in early post- Wisconsin time from ground squirrels crossing the Continental Divide from the southwest to occupy the area north of the Yellowstone River. Chromosomal reorgani- zation in such a small isolated, newly established colony would not then be lost through hybridization with the more nu- merous ground squirrels having the ancestral chromosomal pattern. This “founder” col- ony could then proceed to occupy the empty niche available as the northern Great Plains became ice-free. The first model is supported by the present greatly restricted introgression between 2n = 34 and 2n = 36 populations of ground squirrels, and X and Y chromosome, as well as autosomal re- patterning, which suggests a secondary contact between the two forms differen- tiated as a result of prolonged isolation; the present contact between 2n = 34 and 2n = 36 ground squirrels may well have been established after the Wisconsin glacial period. On the other hand, the absence of this ground squirrel on the Great Plains south of the Yellowstone-Missouri system supports the idea of post-Wisconsin dif- ferentiation proposed in the second model. CONCLUSIONS The biogeographic evidence thus sug- gests that a 2n = 34 ground squirrel from the Great Basin was ancestral, and that the Great Plains 2n = 36 form evolved from it by a dissociative process in which a meta- centric chromosome divided to form two acrocentrics. The fact that true telocentrics were not formed argues against simple fis- sion through the centromere. We are aware that there is a considerable body of evidence that centric fusion is the more common phenomenon in mammals; indeed, definitive cytological evidence for fission is lacking. Hence the possibility that Spermophilus evolution has proceeded from higher to lower chromosome numbers (Nadler, 1966) must be considered. At present, the integrity of the two forms appears to be maintained naturally, by either selection against hybrids and/or an unknown isolating mechanism. In the zone of contact, hybrids are rare compared to parental types, and it is convenient to regard the two forms as semispecies (sensu Short, 1969). If further study verifies that gene flow is as sharply restricted between the two populations as now appears to be the case, and if this restricted gene flow is due to natural selection acting against hy- bridization between the two chromosomal forms, and not merely to temporal or geo- graphic factors, then the distinctness of the 2n = 34 and 2n = 36 forms should be recognized by nomenclatural changes. Tax- onomically, the 2n = 34 populations would then be referable to Spermophilus elegans; 2n = 36 populations retain the name S. 49] 304 richardsonii. The bacula of the two forms are also distinctive; Burt (1960) stated “the structural differences [are] greater than normally found between species.” Ad- ditionally, fleas of the two taxa are dif- ferent; S. richardsonii harbors Oropsylla rupestris, a flea of northem affinities, whereas S. elegans has O. idahoensis, a species common to a number of westem Spermophilus (Jellison, 1945). ACKNOWLEDGMENTS We thank Jeff Greer, Karl R. Hoffmann, and Nancy Nadler for assistance in obtain- ing specimens; Kathleen Harris and Charles F. Nadler, Jr. provided technical assistance. R. Jackson and P. V. Wells, both of the University of Kansas, suggest valuable im- provements in the manuscript, although they do not agree with all of our interpreta- tion. The study was supported by NSF Grants GB 3251 and GB 5676X. REFERENCES Burt, W. H. 1960. Bacula of North American mammals. Misc. Publ., Mus. Zool., Univ. Mich., No. 113. 75 pp. Davis, W. B. 1939. The recent mammals of Idaho. Caxton Printers, Caldwell, Idaho. 400 pp. Durrant, S. D., AND R. M. HAnsEN. 1954. Distribution patterns and phylogeny of some western ground squirrels. Syst. Zool., 3:82—85. FENNEMAN, N. M. 1931. Physiography of west- ern United States. McGraw-Hill, New York and London. 534 pp. FINDLEY, J. S., anD S. ANDERSON. 1956. Zoo- geography of the montane mammals of Colorado. Jour. Mamm., 37:80-82. Hari, E. R., anp K. R. Keutson. 1959. The mammals of North America. Ronald Press, New York, 1:xxx + 1-546, + 1-79. Hansen, R. M. 1962. Dispersal of Richardson ground squirrel in Colorado. Amer. Midl. Nat. 68 :58-66. Hisarp, C. W. 1937. Notes on some _ verte- brates from the Pleistocene of Kansas. Trans. Kans. Acad. Sci., 40:233-237. HOFFMANN, R. S., anp J. K. Jones, Jr. 1970. Influence of late-glacial and post-glacial events on the distribution of Recent mammals on the northern Great Plains. Pp. 355-394 in Pleisto- cene and Recent environments of the Central SYSTEMATIC ZOOLOGY Plains. Dort, W., Jr., and J. K. Jones, Jr., eds. Univ. Kansas Press, Lawrence. 433 pp. HoFFMANN, R. S., P. L. Wricut, anp F. E. Newsy. 1969. The distribution of some mam- mals in Montana. I. Mammals other than bats. J. Mammal., 50:579-604. Howetit, A. H. 1938. Revision of the North American ground squirrels, with a classification of the North American Sciuridae. N. Amer. Fauna, 56. 256 pp. JELLIson, W. L. 1945. Siphonaptera: the genus Oropsylla in North America. J. Parasit., 31: 83-97. LECHLEITNER, R. R. 1969. Wild mammals of Colorado. Pruett Publ. Co., Boulder, Colo. XIII. 254 pp. LemMkKE, R. W., W. M. Latrmp, M. J. Tipton, AND R. M. Linpvautu. 1965. Quaternary geology of northern Great Plains. pp. 15-427 in The quaternary of the United States, H. E. Wright, Jr., and D. G. Frey, eds. Princeton Univ. Press, Princeton, N. J. 922 pp. Lewis, H. 1966. Speciation in flowering plants. Science, 152:167-172. MattTHey, R. 1963a. Polymorphisme chromo- somique intraspécifique et intraindividual chez Acomys minous Bate (Mammalia-Rodentia- Muridae ) Chromosoma, 14:468—497. MatrHey, R. 1963b. Polymorphisme chromo- somique intraspécifique chez un Mammifére Leggada minutoides Smith ( Rodentia-Muridae ). Rev. Suisse Zool., 70:173-190. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge. xiv + 797 pp. MereiaM, C. H. 1891. Results of a biological reconnoissance of south-central Idaho. N. Amer. Fauna, 5. 127 pp. Naber, C. F. 1964a. Chromosomes and evolu- tion of the ground squirrel, Spermophilus rich- ardsonii. Chromosoma, 15:289-299. Napier, C. F. 1964b. Chromosomes of the Nevada ground squirrel Spermophilus richard- sonii nevadensis (Howell). Proc. Soc. Exper. Biol. Med. 117:486—488. Naver, C. F. 1966. Chromosomes and _ syste- matics of American ground squirrels of the subgenus Spermophilus. J. Mamm., 47:579-596. NapDLer, C. F. 1968a. Chromosomes of the ground squirrel, Spermophilus richardsonii aureus (Davis). J. Mamm., 49:312-314. Naber, C. F. 1968b. The chromosomes of Spermophilus townsendi (Rodentia: Sciuridae) and report of a new subspecies. Cytogenetics, 7:144-157. SHort, L. L. 1969. Taxonomic aspects of avian hybridization. Auk, 86:84—105. THAELER, C. S. 1968. Karyotypes of sixteen populations of the Thomomys talpoides complex of pocket gophers (Rodentia-Geomyidae ). Chromosoma, 25:172-183. 492 GROUND SQUIRREL CHROMOSOMAL DIVERGENCE 305 WAHRMAN, J., R. Gorrern, anp E. Nevo. 1969. ZmmMeRMAN, E. G., AND M.R. Lee. 1968. Vari- Mole rat Spalax: evolutionary significance of ation in chromosomes of the cotton rat, Sig- chromosome variation. Science, 164:82-83. modon hispidus. Chromosoma, 24:254—250. We tus, P. V. 1970. Postglacial vegetational history of the Great Plains. Science, 167:1574— 1582. Manuscript received June, 1970 493 VARIABILITY IN CHARACTERS UNDERGOING RAPID EVOLUTION, AN ANALYSIS OF MICROTUS MOLARS R. D. GUTHRIE University of Alaska, College, Alaska Accepted October 31, 1964 Information amassed by animal breeders has aided considerably the understanding of the genetic changes that accompany pheno- typic population changes through time. In spite of genetic inferences from these artifi- cial selection experiments, there are few studies of genetic and phenotypic changes in characters evolving under natural con- ditions. Because of the scarcity of statisti- cally adequate series of fossils and the in- completeness of knowledge of phylogenetic patterns, the contributions of paleontology to the understanding of evolutionary dy- namics have been far below its potential. However, as phylogenies become better known and series are emphasized rather than types, it is increasingly possible to study the detailed behavior of evolving characters. Findings of these studies, in turn, permit a more critical evaluation of our theoretical models. One of the critical areas of evolutionary research is the behavior of the intrapopula- tional variation of a character when it is undergoing change. An understanding of the changes in genetic variation as the pop- ulation moves from one mean to another is central to any investigation involving evo- lutionary mechanics. Lerner (1955) listed as one of the significant landmarks of population genetics the discovery of the great genetic reserves in natural popula- tions, yet this high potential genetic vari- ation is usually associated with relatively low phenotypic variation. According to our present concepts, sustained intensive direc- tional selection would decrease and even- tually exhaust this residual store of genetic variance. In reality the situation is never brought to this extreme since evolution, even at its most rapid pace, is slow com- pared to changes produced by artificial se- lection. However, the problem of the elimi- EvotuTion 19: 214-233. June, 1965 nation of genetic variance does have mean- ing at its intermediate stages. It is the as- sumption of many evolutionary thinkers that as the population responds to the pres- sures of directional selection the genetic and phenotypic variation immediately de- creases, discouraging further evolutionary changes proportionally. The findings of this study lead me to take issue with this assumption. Empirical documentation supporting a reduction of phenotypic variation in evolv- ing populations has been discussed by Simp- son (1953) and Bader (1955), although, in their material, the decreases in phenotypic variation were slight. Since evolutionary change in both cases was taking place at only a moderate pace, an examination of a more rapidly evolving group would theoreti- cally provide greater clarification as the in- terrelationships would be accentuated by the more intense selection pressures exerted over a shorter period of time. This study is an examination of such a rapidly evolv- ing group. The variation of a suite of evolving characters has been compared to the variation of their more stable homo- logues. One of the best examples of rapid evolu- tion documented in the mammalian record has been chosen for this investigation. The setting for this rapid radiation is the late Pliocene and Pleistocene, a time of major ecological upsets, rapid introduction of new habitats, periodic invasions of new terri- tory, and novel associations of faunas. The microtine rodents changed so rapidly dur- ing this time that they are used as one of the better markers for correlation of the Pleistocene stages (Hibbard, 1959). Microtines are well represented in the fossil record, and as a result of their generally high population densities, where present, 214 494 VARIABILITY IN MICROTUS MOLARS fossils are usually abundant. The micro- tines have undergone a major adaptive shift from the seed—fruit diet of the typical crice- tine to a bark—grass diet. This change has been accompanied by a characteristic in- crease in the complexity of the dentition, which is the most durable portion of a mam- mal and also the part most frequently pre- served. The microtines have developed in this short period of time a tooth complexity comparable to that which the Equidae achieved throughout the entire Tertiary. Bader (1955) suggested about two million years as the average duration of a species of oreodont. This length of time would be too conservative for genera of microtines. Preliminary studies indicated that the teeth and the areas of the particular teeth which are undergoing phylogenetic change (more variable interspecifically and inter- generically) are also those which are more variable intraspecifically and intrapopula- tionally. Two abundant species of Microtus that represent two minor grades of tooth complexity were selected, the extinct M. paroperarius from the Kansan glaciation and the recent species M. pennsylvanicus, first known from the IIlinoian. It should be emphasized that, unlike studies of fossil material which compared the variation between rapidly and slowly evolving lines for a variety of characters, this study was a comparison of characters within populations. The variation of tooth characters that are undergoing rapid evolu- tion was compared with the variation of their serial homologues which are main- taining a fundamentally stable morphology. The hypothesis examined was that highly variable characters are not ipso facto ves- tigial. Quite the contrary, some of these characters have recently been, or are yet being, subjected to directional positive se- lection. Stated in another way, characters undergoing directional selection do not ex- hibit the expected phenotypic trend toward homogeneity; rather, they retain the same magnitude of variation or even increase that magnitude. A correlate of this state- ment is that those characters which are 215 more variable between groups at a lower taxonomic level are also more variable within these groups. As it is difficult to speak of selection in- tensity in wild populations, a phylogenetic unidirectional change in a mean will be equated in the ensuing discussions with se- lection response. This implied association does not necessarily follow since migration, inbreeding, and distortion of the gene pool due to random fluctuations alone may also cause a movement of the population mean. In the case of the microtine tooth varia- tions, these exceptions to the assumption are probably not involved. The tooth evo- lution follows a syndrome of related adap- tive changes of which increased tooth com- plexity is but one facet. According to our present knowledge, only selection can be held responsible for directional change of this type and magnitude. EVOLUTION OF MICROTINE MOLARS Most of the radiations involving grazing mammals began in the Miocene with the formation of the temperate and boreal grasslands. For some unknown reason the microtine radiation, involving a dietary shift from the fruiting part of the plant to the vegetative part, lagged until the late Pliocene. As in many other radiations in- volving the exploitation of a coarser diet, the low-crowned tuberculate teeth changed into complex high-crowned prismatic teeth to compensate for the increased rate of at- trition. The microtine molar crown consists of a wide enamel loop at one end with alter- nating left and right triangles following. These triangle-like extensions are termed salient angles and the troughs between are the re-entrant angles (Fig. 1). The crown pattern of the upper molars is oriented posteriorly (the loop on the anterior part of the tooth) while the crown pattern of the lower molars is just the reverse. Except for this reversal the tooth pattern of the uppers and lowers is fundamentally the same so that M? has approximately the same shape as Mz except that the loop of 495 216 UPPERS LOWERS re-entrant angle salient angle posterior loop Fic. 1. A pictorial representation of the 42 mea- surements taken on the upper and lower teeth in two species of Microtus. Width measurements are numbered serially from the loop. Anterior and posterior lengths of each tooth are designated by (a) and (p) respectively, and the entire length of each tooth by (L). the former is anterior and that of the latter posterior. In the upper molars the enamel border of the salient angles is convex on the anterior edge and concave on the posterior; in the lower teeth the pattern is reversed. Moving the teeth anterior—posteriorly pro- duces a self-sharpening system of opposed shearing blades. Microtine molars have become more com- plex by the addition of salient angles and in the more advanced forms the teeth are quite elaborate. Phylogenetically the up- pers add on to the posterior margins of the teeth and the lowers to the anterior. As a consequence, the posterior margin of M?® and the anterior margin of M, are the most variable between taxa. There have been numerous changes in all of the molar crowns although M?, Me, and M3 are more con- R. D. GUTHRIE stant than any of the other teeth. M3 does vary in form intergenerically; perhaps this is a result of the position of the incisor root as it arcs past M3. In some genera the in- cisor passes between M3 and the two an- terior molars and in other genera it does not. The addition of triangles is accom- plished in M®? and Mj, as illustrated in Fig. 2, by an increased penetration of the re-entrant angles in the trefoil or the pri- mordium at the variable end of the tooth. In the other molars the addition of tri- angles is accomplished by a lateral pinching off, phylogenetically speaking, of a bud from the last triangle (see M? in Fig. 2). M® and M, maintain a labile primordium at the changing end, whereas this analo- gous area in the other molars abuts against the stable loop of the following tooth and cannot maintain such a variable structure, but has to resort to the use of the last salient angle if new angles are to be added. The addition of salient angles has taken place throughout the late Pliocene and Pleistocene, but it would be naive to con- sider the whole subfamily as being con- stantly driven unidirectionally by a bom- bardment of selection pressures toward a new adaptive peak. Some groups within the subfamily have become stabilized inter- mediates between the two adaptive ex- tremes. There is almost a whole generic continuum, even in the living forms, from the simple crushing bunodont dentition to a complex continuously growing hypsodont type. Within the various lines of descent there have been irregular increases in the rate of acquiring tooth complexity. Also there has been a varied differential between lines in the attainment of complex hypso- dont molars. Microtine evolution is com- parable to the evolution of horse cheek teeth through the Tertiary, where the more progressive grazers were often flanked by browsing groups with dentition of an an- cestral pattern. It is not intended to be implied that the teeth are the only or even the major char- acters undergoing change. Emphasis has been put on dentition in this treatment as 496 VARIABILITY IN MICROTUS MOLARS Fic. 2. the two species of Microtus: (A) M. paroperarius, (B) M. pennsylvanicus. The relatively stable areas are marked with parallel lines, and the variable areas are cross-hatched (see Fig. 1 for orientation). it is one of the few characters which is con- sistently preserved in the fossil record. Al- though character choice in the fossil micro- tines is limited by default, it would have been difficult to have found a more suitable index of adaptive change. MeEtTHops, MATERIALS, AND MEASUREMENTS Samples of multiple series were used in this study to investigate the horizontal (in- traspecific) and vertical (phylogenetic) 217 raauean-/, CoooTy Ty A semischematic illustration of the extent of tooth crown variations found in species uniformity of the differential tooth variations. The main comparison is of in- dividual variation within each series and not between series. The material is treated as four samples. The first sample repre- sents the extinct M. paroperarius, which occurs only as a fossil. Samples two, three, and four are of the Recent meadow vole, M. pennsylvanicus. Sample two is one series with the sexes combined and the last two samples are another series with the sexes treated separately. These two species 497 218 probably represent one evolutionary line; at least M. pennsylvanicus had to pass through the morphological stage repre- sented by M. paroperarius. The series of M. paroperarius was ob- tained from the collections of the University of Kansas Museum of Natural History. This species was first described by Hibbard (1944) and was considered in more detail, including a qualitative analysis of the intra- populational variation, by Paulson (1961). The sample was collected by Hibbard from several localities in Meade County, Kansas. These localities all belong to the Cudahy Fauna, which lies just below the Pearlette ash, a petrographically distinct volcanic ash. The Pearlette ash is a widespread Pleisto- cene marker of the non-glaciated areas in central and western North America and serves to delineate a contemporaneous fauna over a considerable territory. Hib- bard (1944) considers the Cudahy Fauna to be late Kansan in age. It was necessary to use teeth from several localities in order that a statistically ade- quate sample could be acquired. The series of M. paroperarius was taken as a not-too- serious deviation from an approximated population sample since the localities were all within one county and stratigraphically contemporaneous. M. paroperarius is represented by single teeth, although a few remained attached to mandible fragments. The majority of the teeth came from K. U. localities 10 and 17, but a small number were from Locality No. 20. The individual tooth morphology was so characteristic that the individual molars could be easily identified as to up- per or lower first, second, or third molars and separated as to left or right. The sexes were not distinguishable. The measure- ments of the left and right teeth were com- bined to increase the sample size. There was a positive correlation between the fre- quency of the teeth in the collection and their size. M3 was the smallest and most fragile tooth and M, was the largest. There were fewer M3’s than any other tooth in the sample (31) and the My,’s were the R. D. GUTHRIE most numerous (58). This numerical dis- parity could have been due either to the fact that a more robust structure would better survive preservation or that, as fos- sils, a larger individual fragment would be more likely to be detected than a smaller one. The second sample, of the Recent M. penns ylvanicus, was obtained from the Car- negie Museum collections through the Chi- cago Museum of Natural History. This sample was originally collected from the Pymatuning Swamp, Crawford County, Pennsylvania, an area 15 miles long by three miles wide. Goin (1943) included a qualita- tive review of the M® variations of this sam- ple and discussed the locality in more detail. Fifty individuals were used, 25 males and 25 females. The sexes in sample two were combined as in the first sample (M. paro- perarius). The teeth in the second sample, unlike those of M. paroperarius, were all in place in the jaws. Samples three and four are, respectively, males and females of M. pennsylvanicus. There were 40 males and 42 females. This series was borrowed from the University of Michigan Museum of Zoology and was originally collected near the city of Lynd- hurst, Ohio. The sexes were treated sepa- rately to eliminate the variable of sexual dimorphism and to see what changes this dimorphism brought about in the patterns of tooth variations. In this study I treated the teeth as prismatic structures with no ontogenetic variation. This assumption is true for all practical purposes once the individual has passed the early juvenile age. Juveniles can be culled from Microtus samples by the criteria of overall small skull size, lack of suture closure, and lack of parallel-sided molars. The molars continue to grow throughout the life of the adult individual, maintaining an almost constant crown pat- tern. I treated the tooth crown as if it were a two-dimensional surface. This procedure is also not precisely correct. The upper tooth-row surface wears to a slight convex 498 VARIABILITY IN MICROTUS MOLARS profile and the lower conforms to this with a concave profile of the same magnitude. The mean of the greatest distance that the arc deviates from a straight line, intersecting the terminal ends of the arc, is 0.25 mm or 0.041 of the distance of the straight line. From the lateral view the teeth are also curved; the Mi’s have their concave sides anterior and M3’s posterior. The M?’s have only a slight curvature. In most of the teeth there is a dorsoventral twist, so Micro- tus molars may be considered in form as segments of a broad helix. The teeth of this genus are quite small, the whole tooth-row being only about 6 mm long in M. pennsylvanicus. To cope with the problem of measuring teeth of this size in detail, photographs of the tooth crown of the individual teeth in M. paroperarius, and of the whole tooth-row in M. pennsyl- vanicus, were taken through a dissecting microscope. The crown was first oriented at right angles to the ocular, then the camera was mounted and brought into focus. All pictures were taken through the same ocular at the same magnification. These were then enlarged and developed under the same conditions, including film, paper, and enlarger magnification. A note on the technique (Guthrie, in preparation) includes approximations of the errors in the technique at the various steps. The measurements were then taken from the pictures with a dial micrometer reading to the nearest 0.1 mm. With the picture enlargement of 31.8, this resulted in mea- surements to the nearest 3.3 microns. The measurements were quite repeatable. The exterior edge of the enamel was used in all measurements. Pictures of both left and right sides were taken of M. pennsylvanicus. The side with the picture of highest con- trast was used, and, if there was any ques- tion, measurements were taken on both sides. Rarely was there a break or crack on both sides so that no measurement could be taken. Measurements were made as illustrated in Fig. 1. The measurements on the whole were well defined. The only possible ex- 219 ceptions were the anterior part of M, and the posterior part of M*. However, this is a function of their variability in form. Several measurements were used on the anterior part of M, and posterior part of M’, but no one expresses adequately the vari- ation in shape. The width measurements for each tooth are numbered serially from the loop. Con- sequently, the uppers are numbered from anterior to posterior and the lowers from posterior to anterior. The total length is designated by L and the anterior and pos- terior lengths by a and p, respectively. Forty-two measurements were taken on each individual, 20 measurements on the uppers and 22 on the lowers. DISCUSSION OF MOLAR VARIATIONS The variation in M,, M?, and M® is represented in Fig. 2. The teeth viewed from left to right depict the nature and ex- tent of the shape variations present in these samples. In reality, this variation does not fall into discrete classes as portrayed in Fig. 2; rather, each tooth in the figure represents a point along the variation con- tinuum. The most variable portions are cross-hatched to facilitate the comparisons. Notice that in M, the rounded primordium on the lower part, actually the anterior part of the tooth, is utilized to construct new salient angles by the penetration of re- entrant angles into its lateral margins. In the M? a new salient angle is formed by the budding off of the extreme posterior part of the crown, and varies in these sam- ples all the way from absence to almost the size of the other salient angles. M. paro- perarius has only a slight suggestion of this bud in some individuals, with most not having it at all. In M. pennsylvanicus this rudimentary stage is present only at a low frequency, most of the individuals having a well-developed salient angle. The cross-hatched area in the posterior portion of the M® behaves differently than the cross-hatched area in the M,. M® in- creases its number of salient angles phylo- genetically by dropping a bud posteriorly 499 220 R. D. GUTHRIE 1,2,3 Fic. 3. Coefficients of variation (C.V.) of the upper molars of M. paroperarius (sample 1) and M. pennsylvanicus (samples 2-4) ; samples are identified in text. The tongue inserts are equal to two standard errors in each direction. The measurements at the base of each histo- gram correspond to those in Fig. 1. 500 VARIABILITY IN MICROTUS MOLARS 221 ee eC ty ee 123 12 3 ap ap SP C.V. eed ct Oe 3 7 2253 23 ap a p Fic. 4. Coefficients of variation (C.V.) of the lower molars of M. paroperarius (sample 1) and M. pennsylvanicus (samples 2-4) ; samples are identified in text. The tongue inserts are equal to two standard errors in each direction. The measurements at the base of each histo- gram correspond to those in Fig. 1. 501 222 and enlarging it lingually. However, on the labial side, the penetration of the re-entrant angles and the outgrowth of the salient angles act in a manner much the same as in the M,. There is very little difference in principle in the mode of addition of salient angles in any of these teeth, only slight variations in detail. These cross-hatched areas are the ones that vary most between species. For exam- ple, the M® tooth pattern at the extreme right in Fig. 2 is present in only one indi- vidual in the samples of M. pennsylvanicus, but is the most common tooth pattern in M. chrotorrhinus. Komarek (1932) reports a specimen of M. chrotorrhinus which has one less angle in the M® than usual. This specimen would correspond to the most common M. pennsylvanicus pattern. In ad- dition to M. pennsylvanicus, several other species of Microtus have hints of the pos- teriolingual bud on the M?, and in M. cali- fornicus it is of creditable magnitude (Hooper and Hart, 1962). A further dis- cussion of the intrageneric variations in Microtus is given by Hooper and Hart in the preceding reference. There is some overlap in shape between the fossil M. paroperarius and the recent M. pennsylvanicus. Referring to Fig. 2, in M, the third pattern from the left, in M? the second, and in M? the fourth are com- mon to both species. However, it must be kept in mind that the discrete patterns illustrated here are only chosen points along a continuum. The 42 different measurements are repre- sented by histograms in Figs. 3 and 4. The most striking pattern is the high variation in the width measurements in the anterior part of M, and the posterior part of M?. Although this varies slightly in magnitude between samples, the general pattern is much the same. The width measurements of M! have relatively low coefficients of variation, all under six. The M? width measurements also have relatively low co- efficients of variation. The width measure- ment number three of M?, which includes the incipient angle, has a larger coefficient R. D. GUTHRIE of variation than any of the other width measurements of either M! or M?. This is the incipient angle which is predominantly present in M. pennsylvanicus and expressed in some individuals of M. paroperarius as a rudimentary bump. In every case in the upper molars the anterior length is less variable than the posterior length, Fig. 3, (a) and (p) re- spectively. In the case of M?! in samples three and four, which represent males and females from one series, the difference be- tween (a) and (p) is not outstanding. The difference between the coefficients of vari- ation of the anterior and posterior length is greatest in M?, which has no overlap at two standard errors in either direction. The en- tire length measurements (L) of M?! and M* appear to have about the same magni- tude of variation. The length measurement of M? has a larger variation in all cases than either M?! or M?. It will be remem- bered that the upper molars add to the tooth complexity from the posterior mar- gins. From the findings here it may also be stated that these phylogenetically varia- ble posterior areas of the uppers have the greater intrapopulational variability. The uniformity of the four samples would seem to increase with the order in which they are listed, as there are progres- sively fewer collecting restrictions imposed. The fossil M. paroperarius sample was taken from several localities and with some temporal variation involved. The second sample, of M. pennsylvanicus, was taken over a wider territory than samples three and four, which were collected near a small city. Since there is a high interpopulational variation in M. pennsylvanicus, even within the same subspecies (Snyder, 1954), the difference in uniformity of the collecting restrictions might be thought to affect the relative amount of within-sample variation. With but one or two exceptions, the mea- surements did not show this expected vari- ational gradient between samples. There also proved to be no pattern differences of appreciable magnitude between the two sexes of M. pennsylvanicus. 502, VARIABILITY IN MICROTUS MOLARS In the uppers the measurements of M. paroperarius tend to be more variable than the samples of M. pennsylvanicus, especially the posterior part of M® where the co- efficient of variation is about double, at least in the width measurements. In the width measurements of the phylogenetically more stable teeth M! and M? there is no notable difference in magnitude between M. paroperarius and M. pennsylvanicus. The M? widths have a relatively low to moderate variation, with a coefficient of variation of about six or less, and no out- standing pattern within the tooth. Ms width measurements tend to be more vari- able than those of the Mz with the anterior width measurements having the greater variation. The coefficients of variation are very large in the anterior part of M, (note width measurements five, six, and seven). Another peculiarity of M, in M. pennsyl- vanicus is that the width measurements in the midsection of this tooth are less vari- able than either the anterior or posterior ones. Some of the other teeth show this to a minor degree (note M! and M?). In the lowers the anterior length measurements (a) are more variable than the posterior length (p) in every case except the Mo of sample four. Unlike the uppers, the lowers add on to the anterior margins of the teeth, and we may conclude from the coefficients of variation in Fig. 4 that these anterior areas of the lower molars also have the greatest variation. In both the posterior lengths (p) and the whole lengths (L) there is a trend toward greater variation in an anterior to posterior direction in both the uppers and lowers. This is not so well marked in the anterior length (a) measurements. Of the measurements of the entire tooth length, the length (L) of Mz is the most variable in M. pennsylvanicus while the length (L) of M? is the most variable in M. paroperarius. This is a case where the patterns produced by the length variations (L) are somewhat misleading. In M. penn- sylvanicus M® is the upper tooth with the most variation, which both the width and 223 the length measurements suggest. My, on the other hand, is the most variable tooth in form among the lowers. This is evident in the width measurements but does not show up in the length (L) measurements of M. pennsylvanicus. Although My, is the most variable lower tooth it has developed a long stable posterior area which dampens the variations occurring at the anterior part of the tooth, thereby producing a decep- tively low coefficient of variation for the entire tooth length. This effect is not present to the same degree in the M, of M. paroperarius (see Fig. 2). At this early phylogenetic stage the tooth has a rela- tively smaller stable posterior section. Ms; has a relatively higher variability than the other phylogenetically more stable teeth M!, M?, and Mp. It is the one tooth that crosses over the incisor root and has a limited role in adding to the crown com- plexity of the tooth-row, and may even be in a state of reduction in this particular genus. In some other genera of microtines, Dicrostonyx for example, the incisor root does not cross over in this fashion and the Mz; has developed a more complex crown pattern. Also, it is not reduced in size laterally as it is in Microtus. These facts suggest that the peculiar relationship of M3 to the incisor places some limitations on its potential for increased complexity. In many of the cricetines both the upper and lower third molars have undergone considerable reduction; this is not the case in Microtus. Some individuals of M. penn- sylvanicus have a longer M® than M?. In summary then, a quantification in these two species of the molar variability reveals an overall pattern of higher vari- ation in the posterior parts of the upper molars and the anterior parts of the lowers. The greatest amount of variation is present in the anterior end of M, and the posterior end of M*. A direct positive correspon- dence exists between those areas of the teeth which are changing phylogenetically and those which exhibit a greater magni- tude of variation. 503 224 SUPPORTING EVIDENCE The significance of a positive association between the rapidly evolving tooth charac- ters and a relatively high variability in Microtus is dependent upon its general ap- plicability. This may be either a special case or an expression of a more general phenomenon. The following is a presenta- tion of evidence supporting its more general nature. In the microtines this association is not limited to the M. paroperarius—pennsyl- vanicus line, but rather it is a common feature of the whole group. Dicrostonyx has the most complex crown pattern of the sub- family. D. torquatus, the species repre- sented in the second phase of the last glaci- ation (Zeuner, 1958), has a variable ex- pression of new salient angles on the pos- terior margin of M?! and M? and the an- terior margin of Mz and M3. These salient angles are highly variable in their occur- rence, grading to complete absence in some individuals. The characteristic species of the last glaciation, phase one (early Wis- consin), was D. henseli, which did not possess the salient angle or bud as did D. torquatus. This bud seems to be a nascent character developing through the last glacial age. D. groenlandicus, a recent species, has this character present in all individuals. D. hudsonius, a species with a distribution presently limited to the Hudson Peninsula, is a living relict representative of the D. henseli tooth pattern of the early part of the last glaciation. D. torquatus exists as the modern Old World collared lemming. Thus there is a chronological and geographi- cal representation of the stages of develop- ment of this salient angle. The fossil D. henseli and the recent D. hudsonius do not have the salient angle. D. torquatus, both modern and fossil, has a varied expression of the salient angle from absent to fully present (Hinton, 1926). In populations of D. groenlandicus all individuals have it. Some taxonomists give these forms only subspecific status; however, the principle dealt with here remains valid. Kurtén (1959) suggested that the aver- R. D. GUTHRIE age rate of mammalian evolution during the Pleistocene was relatively higher than during the Tertiary. His analysis of the variability in several rapidly evolving groups, widely separated taxonomically, re- vealed an increase in the coefficient of variation in more lines than a decrease. Although his study did not deal in detail with the specific characters which are changing (he used an average of several measurements), it did serve to illustrate that rapidly evolving populations do not all tend toward morphological uniformity. On the contrary, it suggested the opposite. Wright, in the discussion at the end of Kurtén’s paper, proposed that recombina- tion is responsible for this amplification of potential variability. Skinner and Kaisen (1947) noted that while there are few diagnostic patterns in the evolution of Bison cheek teeth, there is a general trend toward the molarization of Py. The metastylid and median labial root of the Py increase in frequency through time. In early fossil Bison these characters are virtually absent and in modern ones almost universally present. The increases in the complexity of P, seem to have oc- curred over a relatively short period of time during the late Pleistocene. Since these evolving areas range from absent to fully developed in some populations during this period of incipiency, the variability is greater than that of the analogous areas of neighboring teeth. Simpson (1937) discussed a sample of 33 Eocene notoungulates, Henricosbornia lophodonta, which he considered to be from one population, since their variation is normally distributed and they are from the same horizon and locality. These were originally described by Ameghino as be- longing to 17 species, seven genera, and three families, principally on the basis of the variation present in the upper third molar. The variations present within this primitive form are characteristic of later species, genera, and families with which Ameghino was familiar. Here is an exam- ple of a considerable amount of variation 504 VARIABILITY IN MICROTUS MOLARS in one population, the elements of which are later characteristic of higher taxa. It would be consistent with the evidence to assume that the tooth is undergoing evolu- tionary change in a manner which contrib- utes to the types characteristic of later higher taxa. Hooper’s (1957) study of the dentition of Peromyscus gives supporting evidence to the main thesis proposed here of rapid evo- lution being accompanied by high pheno- typic variation. A series of P. maniculatus from Distrito Federal, Mexico, for example, has highly variable molars. The mesoloph and mesostyle patterns found in this one series resemble the common patterns of the other 17 species of Peromyscus studied. In other words, the mesostyle and mesoloph patterns observed in 17 species of Peromys- cus are also seen in this single series. P. maniculatus is first known from the Wis- consin age and has expanded its distribu- tion over a considerable part of North America. It is considered to be one of the “younger” species of Peromyscus (King, 1961), and therefore has recently under- gone evolutionary change at the species level. The occurrence of the crochet in horse teeth is another example of an incipient character that is highly variable in the same population (Simpson, 1953; Stirton, 1940). The acquisition of this plication is one of the first features in a general trend toward increased tooth complexity. The crochet, an anastomosing ridge between metaloph and protoloph, shows up in the Miohippus—Parahippus line. It is also pres- ent in some species of Archeohippus and sometimes in the milk teeth of Hypohippus (Stirton, 1940). The incipient crochet juts out as a peninsula or pier from the meta- conular part of the metaloph toward the protoloph. The degree of its development is extremely variable, from absence to a small spur extending halfway across, to a complete connection between the two lophs. The crochet varies both in frequency and extent between populations and within them, occurring in its various stages of 229 representation in individuals of the same species at one locality. Butler (1952), speaking of the molariza- tion of premolars in Eocene horses, stated that the metaconule evolving in the pre- molars is most variable at the intermedi- ate stages of molarization. Wood’s (1962) discussion of the tooth cusp variations in the early paramyid ro- dents showed that the hypocone is added to the tooth by two basically different means. In some forms it is derived from an enlargement of the posterointernal cin- gulum; in others it originates as a division of the protocone. Wood attributed these two distinctly different means of achieving fundamentally the same end product to a general selection toward the development of a posterointernal cusp irrespective of the nature of its origin. The addition of the fourth cusp, hypocone, is a common phe- nomenon in many lines during this part of the Tertiary, and seems to be correlated with the exploitation of more demanding food substances. Wood stated, “There is no question but that all of these variants may occur within a single genus and some- times within a single species.” Here again, when a directional selection pressure is being applied, more phenotypic variation is exhibited in the incipient than in the non- incipient cusps. The lower third premolar is used to char- acterize various genera of fossil rabbits. Hibbard (1963) observed much variation within a primitive rabbit genus, Vekrolagus, and found at a low frequency a pattern of the Ps; that is characteristic of modern genera. The common tooth pattern of Nekrolagus is also found at a very low fre- quency in some modern genera. This com- parative study documents a chronological frequency change in which the early fossil populations have the incipient characters represented at a low frequency and the modern populations at a high frequency. Here is another case in which there is a high variation associated with incipient characters, and the axis of this variation is parallel to phylogenetic change. 505 226 Another opportunity to try the hypothe- sis is on the results of artificial selection experiments. If the hypothesis does ap- proximate the real condition, the character that is artificially selected for or against should behave in a manner similar to the evolving characters that have just been dis- cussed. That is, characters undergoing arti- ficial selection could be expected not to ex- perience a decrease in their phenotypic variation, but to maintain or even increase the variation. MacArthur (1949) selected for large and small size in mice using the weight at 60 days as a measure of size. In the un- selected control the coefficient of variation was 11.1. However, in the strain selected for large size it was 12.8, and in the small line 14.3. Falconer (1955) also selected for large and small size in mice using the sixth week weight as a measure of size. He stated, “The phenotypic variability, also, does not reflect the expected decline of genetic vari- ance, and in addition reveals a striking and unexpected change in the small line.” He further reported that the large line showed a slight increase in variation over the whole course of the experiment, although it re- mained relatively low compared to the vari- ation of the small line. The coefficient of variation in the small line increased to about double the original value between the seventh and ninth generations and re- mained at this high level. The realized heritability remained substantially constant up to the point at which response ceased. This phenomenon, he suggested, was due to the release of genetic variation through recombination. In their selection experiments for wing length in Drosophila, Reeve and Robertson (1953) found that the coefficients of vari- ation at the twentieth to seventy-ninth gen- erations were all below two in the unselected strain and all two or above in the selected strain. The strain selected for long wings showed an increase of about 50 per cent in total variance. They attributed this en- tirely to an increase in additive genetic R. D. GUTHRIE variance, which rose about two and one- half times, while the absolute amount of other genetic variance remained about the same. This led them to suppose that selec- tion for long wing length would be far more effective in the selected than in the un- selected stock. Clayton and Robertson (1957), selecting for low and high bristle number in Drosoph- ila, concluded that ‘Selection had by no means led to uniformity, but in some cases even magnified the total variation.” Robertson (1955) selected for thorax length in three stocks of Drosophila with about the same initial amount of variation. The coefficient of variation in the small lines increased immediately in the first gen- erations and was higher than the control in all three lines, although there were be- tween-strain differences in the pattern of increase in variation. In the large lines the variation fluctuated around that of the con- trol stock. Thus, in the large strains the changes in response to selection occurred without appreciable change in the coeffi- cient of variation, while the variation of the small line increased. Although the changes in variation ac- companying selection response in these ex- periments do not behave in a completely uniform manner, they do maintain and usually increase the initial magnitude of variation. Thus, evidence supporting the association between directional selection and a constant or increased variation is found both in rapidly evolving groups and in artificial selection experiments in which the degree of variational change has been recorded. THE THEORY AND MopDEL The most frequently employed explana- tion for an inordinate amount of variation is vestigiality. In such a case the charac- ters under consideration are not becoming more complex phylogenetically but are de- creasing in pattern complexity. Morpho- logical characters which are in the process of reduction or elimination exhibit more variation than do their more functional 506 VARIABILITY IN MICROTUS MOLARS homologues. This high correlation between vestigial and highly variable characters no doubt influenced Hinton (1926) to believe the microtines to be, in tooth form, degen- erate descendants of the multituberculates and consequently undergoing reduction in tooth complexity. However, there is a time gap in the fossil record of some 35 million years between the multituberculates and microtines. The concept of the vestigial nature of microtine teeth has been perpetu- ated by some mammalogists (Goin, 1943; Hall and Kelson, 1959). But the position that microtines did not arise from a crice- tine stock and have not undergone a gen- eral increase in tooth complexity is untena- ble. Not only does the fossil record support an increase in microtine tooth complexity, but there is an almost complete continuum of recent intermediate forms between the Microtinae and Cricetinae. Vestigiality can be discounted as an explanation of the variation differential in the other examples as well, as these characters are also in- creasing in complexity. Lately, much attention has been given to the loss of buffering capacity against en- vironmental stress as the genome tends toward homozygosity (Lerner, 1954). Since directional selection reduces the amount of individual heterozygosity, the loss of buf- fering would result in a greater magnitude of individual deviation from the mean, in- creasing the phenotypic variation of that population. This process may be the cardi- nal factor involved in an explanation of the phenomenon of an increase in variation ac- companying directional selection. However, there is some discouraging evidence against an explanation of this nature. (1) The in- crease of phenotypic variation becomes evi- dent early in artificial selection (Robertson, 1955) before an appreciable amount of genetic variance could have been lost by selection. (2) A character in which selec- tion has considerably altered the mean can often be returned with little difficulty to the original mean by reversed selection. This reversal could not take place if the population had reached a relatively homozy- 227 gous level for that particular character. (3) A correlate of the latter is that often a substantial heritable component is. still present after the mean has been considera- bly altered by selection (Lerner, 1958). (4) Bader (1962) showed that, in tooth form, inbred mice exhibit slightly less phenotypic variation than wild popula- tions; and the outcrossed heterozygote is less variable than either. (5) If the tooth variation discussed here in Microtus is non- genetic, it is difficult to explain the phylo- genetic increase in tooth complexity, since the most important cause of evolutionary change is selection acting upon heritable variation. From some preliminary crosses of microtines (Steven, 1953; Zimmermann, 1952), it does seem that these variations are heritable. In at least one species of Microtus (M. arvalis) there is also a geo- graphic cline in the frequency of tooth complexity. The variations were classed into two discrete types (simple or com- plex); the frequency of ‘complex’ ranges from five per cent to 95 per cent in the cline from northern to southern Europe (Zimmermann, 1935). The accumulated evidence from breeding experiments suggests, contrary to the “‘wild type” or normality concept, that there is considerable heterozygosity underlying the relatively coherent facade of the phenotype. The variation expressed in the phenotype is only a fraction of the total possible varia- tion present (Mather, 1956). There is a diversity of opinion as to the mechanisms involved in the maintenance of this large amount of potential variability. The posi- tion that the balanced additive factors maintain the stored variability has much evidence in its favor in terms of its general applicability to evolution at the intrapopu- lational level. Stated in more detail, this position asserts that there exist balanced systems of linked heterozygous polygenes structurally associated and maintained by selection and perhaps also by decreased recombination. Delayed responses to selection are best accounted for on the basis of genetic link- 507 228 age. A rather common phenomenon in ex- perimental breeding is for a selected strain to reach a plateau of response only to have it resume progress after a period of relaxa- tion of the selection pressures. The most plausible explanation of this phenomenon is linkage disassociation; the various ele- ments are unable to segregate out im- mediately because of linkage restrictions (Mather, 1949). The ineffectiveness of ex- periments to reduce the variation by selec- tion for intermediates (Lerner’s type II se- lection, Lerner, 1958; Falconer, 1957), and the ineffectiveness of selection for the ex- tremes to alter the variation (type III se- lection, Falconer and Robertson, 1956) both suggest that the additive genetic ma- terial resides in balanced linkage groups. Structural change, which often inhibits crossing over, may establish an isolation of segments of the chromosome where crossing over is likely to occur only with configura- tions of that same type; however, the gen- eral importance of this mechanism is still not clear. As well as promoting these de- vices that inhibit recombination, selection can operate directly to maintain these blocks intact (Lerner, 1958) and this is probably the most important mechanism. Carson (1959) reports that most natural inversions are heterotic when removed from nature to the laboratory culture, and that strains derived from a single pair of wild flies retain with extreme tenacity most of their initial inversion variability. The advantages of a system of balanced linkage groups are multiple. The popula- tion can maintain a high degree of hetero- zygosity in many individuals without the rigorous selection required if these elements were segregating at random. The close linkage association also serves as a buffer against random fluctuations away from the optimum. And perhaps most important, it holds genetic material in reserve, thereby maintaining an evolutionary plasticity. There is evidence that integrated chro- mosome segments are important in the as- sociation or correlation of continuously dis- tributed characters, and that they behave R. D. GUTHRIE in a manner similar to single independent genes acting pleiotropically. To resolve or disassociate the correlation of two charac- ters by selection would produce strong evi- dence for linkage. Such disassociation has been accomplished (Mather and Harrison, 1949; Mather, 1956). Correlation due to pleiotropy is, of course, more resistent to evolutionary change than the more labile system of linkage groups. Linkage groups can originate or be disposed of by the selec- tion for various recombination and struc- tural patterns. It would be a slow process for the population to await a new mutation at one locus which acted upon the desired characters in exactly the right magnitude. Selection can maintain a frequency of bal- anced genetic material within each chromo- somal block or “internally” at levels that insure a considerable proportion of “‘rela- tionally” balanced, or heterozygous, indi- viduals in the population. As long as this block remains intact it will carry reserves of variability which may be released and made available for segregation by crossing over. With selection against the cross- overs, this residual genetic variability can be maintained (Lerner, 1958). In order to maintain the internally balanced linked groups a selection intensity would be re- quired equivalent to the frequency of cross- overs which deviate from the balanced con- figuration (Falconer, 1960). The increase in variation of evolving characters may be further enhanced when an interbreeding population experiences the stress of two selective optima. This condi- tion would occur in most evolutionary changes when the group is partially exploit- ing two adaptive zones. Thus, a character in transition may be expected to experience some reduction in stabilizing selection along its axis of change. The high variation usually associated with vestigiality can also be accounted for in the context of this theory. A vestigial character is in essence an evolving charac- ter, as reduction plays a great part in evo- lutionary change. According to the ex- planation given for the greater amount of 508 VARIABILITY IN MICROTUS MOLARS variation in evolving characters, the stored variability is maintained in a linked system by stabilizing selection. When this balance is altered by directional selection, the vari- ability is released. Due to its decreasing functional role, the variation of a vestigial character would also be compounded by a decrease in stabilizing selection. Carson (1955), in his discussion of the genetic composition of marginal popula- tions, surmised that, since the marginal populations contain fewer inversions than central populations, the more stringent selection on the periphery is against the heterotic groups which predominate in the central population. These findings are in agreement with the idea expounded here, that directional selection away from the mean is selection for the breakdown of present linkage configurations. Carson fur- ther reported that when strong artificial selection was applied to both marginal and central population lines, the marginal lines showed the greater initial response. This difference would exist if the genetic ma- terial has been made available for segrega- tion in the marginal populations by the breakdown of the linkage groups. Reeve and Robertson (1953), selecting for wing length in Drosophila, found that the selected strain showed an increase in additive genetic variance of 250 per cent, all other genetic variance remaining about the same. They further suggest that selec- tion for long wing length would be more effective in the selected than in the un- selected stock. Robertson (1955) states: “Selection generally leads to an increase in variance which appears to be largely due to the increased effects of genetic segregation and this constitutes an aid to selection progress.” This release of additive genetic variation provides a mechanism whereby directional selection, in continuously distributed poly- genic systems, increases its own resolving power. Selection against the mean and its present balance situation is selecting against the present linkage configurations, which results in a breakdown of these integrated 229 units. The genetic components are then re- leased and made available for novel segre- gants hitherto unavailable. The conse- quence of this is an increase in phenotypic variation, which is heritable in an additive fashion. As the amount of variation is a determining factor of the effectiveness of selection, in conjunction with selection in- tensity and heritability, further selection gains are facilitated. To set up a simple visual model of this theory let us suppose, as is expressed in Fig. 5, that there is a series of loci with alleles acting in an additive fashion either to the left or right of the mean. Loci a, b, c, and d control the size of character X and e, f, g, and h control Y. The contribution of each allele is specified. Further, suppose these are balanced “internally” and “rela- tionally,” with an equal frequency of each linkage group. The mean will be consid- ered as zero with the deviations from it in both positive and negative directions. A stabilizing selection for the mean would cull out deviants, the crossovers, from this configuration. The genetic material present is potentially able to produce an individual representative of any point in the figure, but this particular linkage configuration limits the phenotypes to a coherent cluster around the mean. The broken circle repre- sents a variation of two standard deviations from the mean, if each locus were acting individually with an equal frequency of each allele. The linked configuration, how- ever, would produce a population with a lower variation, expressed here at two stan- dard deviations by the solid inner circle. If a new adaptive optimum (Xe) were created with a consequent directional selec- tion of moderate magnitude exerted on the distribution, the linkage groups would be selected against by a selection for the cross- overs in the direction of the new adaptive optimum, resulting in a parual breakdown of the coherent phenotype. A structural association of the loci con- trolling the two characters (Fig. 6) would result in their correlation. The points all fall along the diagonal axis between +2 509 230 (+) 3 of =< (@) aoa 0 Fic. 5. R. D. GUTHRIE =A ay bg cy dp ey fy By hy ie a? by i) qy 2) fy 82 hy ~ \ \ = \ a=0.5 \ b=1.0 \ G0s5 \ adi= 120 ! e=0.5 ! f =1.0 : 2 =i)0%5 phate sub1=(—) 7) sub2= (+) CE) An elementary model of the non-correlated case of two characters X and Y, where low phenotypic variation is maintained by selection for the linkage configuration represented in the upper right. With equal frequencies of each linkage group the variation of the population, at two standard deviations, would be circumscribed by the solid circle. The dashed line represents the same loci with no linkage. Selection for X2 would increase the variation as the linkage configuration would be selected against. and —2 units, as shown by the ellipse. If one were to think in terms of the major axis of variation as size, this provides a rela- tively constant individual shape throughout a population in which the individuals are varying in size. As in Fig. 5 it will be noted that an imposed directional selection will produce an increase in variation. Even directional selection parallel with the main axis of size will increase the variation. The greatest increase in variation, however, would be produced by a selection pressure at right angles to the principal axis of vari- ation, toward Xs, which would be selection for shape changes. The long-term effect of this type of selection would be twofold: (1) an increase in phenotypic variation, and (2) a decrease in the correlation of char- acters X and Y. Unlike the situation in Fig. 5, if a selection pressure is exerted on only one character (perpendicular to the scale of the other), the second character is also initially affected. However, it is an inherent mechanism of the model that the linkage which provides the correlation of the characters will be selected against when only one character is subjected to direc- tional selection. This system then would further contribute to evolutionary plas- ticity. 510 VARIABILITY IN MICROTUS MOLARS ~< jo) peel 2 aah 40) oy Iai ay bo eyfp Cy dy By hy ay by Cn fy = Ca dy Bghy a=0.5 b=1.0 c=0.5 d=1.0 e=0.5 f=1.0 g= 0.5 esse sub 1 = —) X Supe? = ce) Fic. 6. Same as Fig. 5 except that characters X and Y are now correlated due to the linkage asso- ciation. This new linkage configuration maintains a coherence differentially on the size and shape axes. Selection toward X2 would considerably increase the variation along the shape axis. I do not wish to imply that the theory expressed here accounts for all the various behavior exhibited by residual genetic varia- tion. Rather, I have investigated one aspect, the association of directional selection and the maintenance or increase of the initial phenotypic variation, and have hopefully offered a plausible explanation, which will be further explored soon by breeding experi- ments with Microtus. SUMMARY This is a study of the intrapopulational variability present in the dentition of two species of Microtus, and the more general questions arising from it. The central thesis is that quantitative characters undergoing rapid evolution do not show the decline in phenotypic variation predicted by our pres- ent evolutionary concepts. On the contrary, the variation is maintained and usually in- creased. Of the two species used, the fossil species is thought to be ancestral to the modern meadow vole; thus the study materials com- prise an evolutionary line with two grades of tooth complexity represented. In the molar crowns of both species, the areas which are changing phylogenetically are those which vary most within the popula- tion. Evidence from other sources in which characters are undergoing directional selec- 511 232 tion, both evolutionary and artificial, sug- gests that a greater variation in characters undergoing directional selection is a general condition. | A theory to account for association be- tween rapidly evolving characters and a relatively higher amount of phenotypic variation is that the coherence of the popu- lation around the mean is due to balanced heterozygous linkage groups and that with the application of directional selection this organization is partially broken down. The genetic variation is then released and made available for recombination. The relatively high variability associated with vestigial characters is also fitted into the context of the theory. The theory suggests that direc- tional selection on continuously distributed characters increases its own effectiveness. ACKNOWLEDGMENTS I wish to express my appreciation to Dr. E. C. Olson, University of Chicago, the chairman of my graduate committee, for his encouragement and assistance with the presentation. Thanks are also due to Dr. Vernon Harms and Dr. Brina Kessel, Uni- versity of Alaska, for their helpful criti- cisms of the manuscript. My deepest grati- tude goes to Dr. R. S. Bader, University of Illinois, for the many stimulating discus- sions which were to form the nucleus of my interests in evolutionary mechanisms. I wish to thank also those in charge of collec- tions at the University of Kansas Museum of Natural History, University of Michigan Museum of Zoology, Carnegie Museum, and Chicago Museum of Natural History for the use of the specimens. LITERATURE CITED Baper, R.S. 1955. Variability and evolutionary rate in oreodonts. Evolution, 9: 119-140. -——. Ms. Phenotypic and genotypic variation in odontometric traits of the house mouse. (Manu- script submitted for publication.) Butter, P. M. 1952. Molarization of premolars in the Perissodactyla. Proc. 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Development and behaviorial evolution in Peromyscus. Pp. 122-147 in W. F. Blair (ed.), Vertebrate Speciation. Univ. of Texas Press, Austin. Komarek, R. V. 1932. Distribution of Microtus chrotorrhinus, with description of a new sub- species. J. Mamm., 13: 155-158. Kurrten, B. 1959. Rates of evolution in fossil mammals. Cold Spring Harbor Symp. Quant. Biol., 24: 205-215. LERNER, I. M. 1954. Wiley, New York. 1955. Concluding survey. Cold Spring Harbor Symp. Quant. Biol., 20: 334-340. Genetic homeostasis. John 512 VARIABILITY IN MICROTUS MOLARS 1958. The genetic basis of selection. John Wiley, New York. MacArTHuR, J. W. 1949. Selection for small and large body size in the house mouse. Genetics, 34: 194-209. MATHER, K. 1949. thuen, London. 1956. Polygenetic mutation and variation Biometrical genetics. Me- in populations. Proc. Royal Soc. London, 145: 293-297. Martuer, K., and B. J. Harrison. 1949. The manifold effect of selection. Heredity, 3: 1- 52, 131-162. Pautson, R. G. 1961. The mammals of the Cudahy fauna. Papers Michigan Acad. Sci., Arts, and Letters, 46: 127-153. Reeve, E. C. R., anp F. W. Rosertson. 1953. Studies in quantitative inheritance II. Analysis of a strain of Drosophila melanogaster selected for long wings. J. Genetics, 51: 276-316. RosBertson, F. W. 1955. Selection response and the properties of genetic variation. Cold Spring Harbor Symp. Quant. Biol., 20: 166-177. Suupson, G. G. 1937. Supra-specific variation in nature and in classification. Amer. Nat., 71: 236-276. 513 233 1953. The major features of evolution. Columbia Univ. Press, New York. SKINNER, M. F., anp O. C. Katsen. 1947. The fossil Bison of Alaska and preliminary revision of the genus. Bull. Amer. Mus. Nat. Hist., 89: 127-256. Snyper, D. P. 1954. Skull variation in the meadow vole (Microtus pennsylvanicus) in Pennsylvania. Ann. Carnegie Mus., 33: 201- 234. STEVEN, D. M. 1953. Recent evolution in the genus Cleithrionomys. Symp. Soc. Exp. Biol., 7: 310-319. Srirton, R. A. 1940. Phylogeny of the North American Eguidae. Univ. California Publ., Bull. Dept. Geol. Sci.. 25: 165-198. ZEUNER, F. E. 1958. Dating the past. Methuen, London. ZIMMERMANN, K. 1935. Zur Rassenanalyse der mitteleuropaischen Feldmause. Arch. Natur- gesch., N. F. 5. 1952. Die simplex-Zahnform der Feld- maus, Microtus arvalis. Pallas. Verh. Deut. Zool. Ges., Freiburg. Sonderdruck aus Z. f. Sdugetierkunde Bd. 32 (1967) H. 3, S. 167—172 Alle Rechte, auch die der Ubersetzung, des Nachdrucks und der photomechanischen Wiedergabe, vorbehalten. VERLAG PAUL PAREY : HAMBURG1 _: SPITALERSTRASSE 12 © 1967 Verlag Paul Parey, Hamburg und Berlin Evolutionary adaptations of temperature regulation in mammals! By L. JANSKY Eingang des Ms. 25. 10. 1966 Generally speaking, adaptations may take place either during individual life of animals (acclimations and acclimatizations), or they may be specific to certain species (evolu- tionary adaptations) (HART 1963b). They may be realized by different mechanisms with different degree of efficiency, however the aim of all adaptations is essentially the same — to reduce the dependence of animals on environmental conditions and thus to increase their ecological emancipation. The study of physiological mechanisms of adaptations is therefore of great ecological importance since it helps us to elucidate physiological processes influencing limits of distribution of different species and having a profound effect on the quality or density of animal populations. The comparison of individual and evolutionary adaptations permits us to trace the evolutionary progres- sive physiological processes and to contribute to the problems of phylogeny. In lowered temperatures mammels tend to lose heat. Theoretically, they can prevent hypothermia either by increasing heat production in the body or by reducing heat loss from the body to the environment. Heat production is realized by shivering; heat conservation may be manifested by reducing the body surface, by improving its insu- lation qualities and by decreasing the body—air temperature gradient according to formula: Tp —-Ta H=K ae (1) (Hart, 1963b) Z COLD ADAPTED S NT Ty, WARM ADAPTED Q shivering | frm Im 8 UU IA & 1 l | nonshivering = shivering il | | | thermogenesis HTT EEE = NANA VU ANJULUUAHITT L a ef a SacGe ye 1690 +20°C > : lower critical temperature cS | | ig i A i 1 / > ' 4 a) ie) a) Fig. 1. Scheme of heat production of rats adapted to warm (30° C) and cold (5° C) environments. According to Hart & JANsky, 1963 1 Presented at the 40th meeting of the German Mammalogical Society in Amsterdam. 167 514 168 L. Jansky INSULATION °C/CAL/M’?/HR S ~ ~ (en S nN 9S (=) @® = ies rem" DEER MOUSE x eo w ae ss S e LEMMING = Slo ) ee 00 000 00 QRS WOLF S| Gs) e@ e@ e @ oe) BLACK BEAR eo = ODN RES CGS POLAR BEAR S S S Fig. 2. Seasonal changes in fur insulation in various mammals (Hart, 1956) (H = heat production, K = a constant representing the body surface area, Tp = body temperature, T, = air temperature, I = insulation qualities of the body surface.) Similary, the adaptations of temperature regulation to cold can be realized either by increasing the capacity of heat production or by mechanisms leading to reduction of heat loss from the body. The adaptation to cold appears as a shift of the lowest temperature limit animals can survive (lower critical temperature). In our earlier work we have shown that the individual adaptations are manifested predominantly by an increased capacity of heat production owing to the development of a new thermogenetic mechanism — called nonshivering thermogenesis (HART, JANSKY 1963). Physiological background of this phenomenon consists in an acquired sensitivity of muscular tissue to thermogenetic action of noradrenaline liberated from sympathetic nervous endings (HsiEH, CARLSON 1957). Nonshivering thermogenesis potentiates heat production from shivering and in rats shifts the lower critical temperature for about 20° C (from —18° C down to — 37° C; Fig. 1). Mechanisms controlling heat loss by changes in body surface area or by changes in body-air temperature gradient are not common in individual adaptations. On the other hand it is well known, that certain species can improve body insulation in winter 515 Evolutionary adaptations of temperature regulation in mammals 169 season. However, this phenomenon becomes functionally justified only in animals of creater size (size of fox and larger; Fig. 2. Hart 1956). The individual adjustments with the aid of nonshivering thermogenesis are encoun- tered both in acclimations under laboratory conditions and in seasonal acclimati- zations induced in the same species under natural conditions. They are undoubtelly very efficient and biologically important. On the other hand, from the ecological point of view, they have also their negative side. The increased heat production results in higher demands for energy restitution in the body, which is attained in cold adapted animals by an increased food consumption. As a result, individuals adjusted this way become more dependent on the quantity and availability of food and they are forced to use more effort to provide it. The reduced dependence of animals on temperature factors is thus substituted by increased dependence on food factors. Contrary to individual adaptations, in evolutionary adaptations mechanisms lea- ding to the reduction of the heat loss are greatly emphasized. Their importance consists in the fact that they save energy for the organism and have lower demands to its restitution in the body. This fact is obviously evolutionary very important — in the processes of phylogeny there occurs natural selection of those individuals that are less impeded by the lack of food, often occuring in nature. Evolutionary adaptations are realized in the first place by an increased insulation of the body cover (fur, Fig. 3). This adjustment, typical for arctic animals, can reduce the heat loss so efficiently, that even considerably reduced ambient temperatures (down to — 50° C) do not result in an increased heat production in larger animals. (Fig. 4; SCHOLANDER et al. 1950a, b). The same role plays a thick layer of subcutaneous fat which appears in some mammals, such as seal and swine. The insulation qualities of this fat layer can be increased by an active restriction of the blood flow to this area. This results in superficial hypothermia, which also efficiently prevents the heat loss (IRVING 1956). Animals endowed with superficial hypothermia have normal thermogenetic abilities. However, compared to the species from tropical regions with little insulation and to arctic species with great surface insulation they show a reduced sensitivity 4 of afferent sensory input = jajguy_ ATION y to temperature stimuli 40 | ys Cag ae (Fig. 5). [WATT 7 DM 737° CAL M? 24uRS- PC GR]-O7 A tendency to reduce ye heat loss by reduction of Ye AS DAL sHeep 7-06 the body surface area ; may be considered as a ee Eau OnE another type of evolutio- GRIZZLY BEAR nary adaptations. This phenomenon occurs in Rooath Gala ar WO. animals living perma- 20 nently in cold climate, ) mil SOARS HEAP 03 which are generally lar- ; gerand haveshorter body SNE een appendages than animals 4Q Sauere SEXS paces ane 4-02 from tropical zone (BERG- NS cain a : MANN’s and ALLEN’s ru- nada | 4.01 les). Both the validity and @ pee ane we / ICE WATER : : tos § BLACK SURFACE } the physiological signifi- g $8 fas cance of these rules have O 10 20 30 40 50 60 70 80 9 been recently questionend by several workers, how- ever. THICKNESS IN MM Fig. 3. Insulation in relation to winter fur thickness in arctic and tropical mammals (SCHOLANDER et all., 1950 b) 516 170 L. Jansky MAMMALS ARCTIC TG YeBELLULL// jj TRL) /£& i 9 SLU ///17) My 200} Mj Wy 2 ME TABOL/ISM ay BESS SSS S BESS SJ SINS Ae = a TROPICAL 100+ ee _ BASAL METABOLIC RATE = 100 ___ OBSERVED ~~ - EXTRAPOLATED ° it 1 aes 1 ae eee is — pes i -70 “Lowest -50 -30 -10 10 307 TEMP ON EARTH BODY TEMP AIR TEMPERATURE IN °C Fig. 4. The effect of environmental temperature on metabolism of arctic and tropical mammals (SCHOLANDER et all., 1950 a) The reduction of heat loss by changing the body-air temperature gradient can be realized either by active choice of higher environmental temperature or by consi- derable lowering of body temperature. It is generally recognized that the active choice of the environmental temperature occurs by seasonal migrations and by changes in patterns of daily activity. It was INFANT sees 8 300 THICK - FURRED ANIMALS, oat ~ I —/Y ag WHITE RAT HOSEA NS 5 200 x SWINE Se >= n wk ‘NS | = SEAL = p 9 2% ge or AR EK 4ooL4 en 6n'5e Ww SEAL fs) ae ce a) ° 0 10 20 30 SKIN TEMP 4 @ Fig. 5. Heat production as a function of skin tempera- ture under fur of the back for a series of mammals (Hart, 1963 a) 517 found that different species of voles and shrews transfer the peak of daily activity to war- mer part of the day in a cold weather (JANskKy & HAanAk 1959). The mechanisms leading to reduction of body-air tempera- ture gradient by lowering of body temperature are especially developed in hibernators. Ac- cording to the latest view hiber- nation is not considered as a lack of temperature regulation rather as a special adaptation of thermogenetic processes. There are two reasons for that: first, hibernators have the same capa- city of heat production as other hemeotherms of similar size (see JANSKY, 1965) and second, the entering, the arousal and the deep hibernation are under remarkably precise physiological control (see LyMAN, 1963). This indicates a leading role of central nervous system in controlling hibernation, which is adapted to hypothermal con- Evolutionary adaptations of temperature regulation in mammals Vil ditions and it is functional at all levels of body temperature. This adaption has certainly its metabolic background, however only little is known about this phenomenon so far. The control of entering into hibernation is realized by the active inhibition of shivering heat production by signals from subcortical centres of the brain. Simultane- ously with the decrease in shivering an active inhibition of the activity of the sym- pathetic nervous system also takes place, which is manifested by the reduction of heart rate and by vasodilatation. These changes facilitate the lowering of body temperature of animals which is realized successively in the form of “undulating” cooling so the organism can slowly prepare to hypothermia (Fig. 6). Nervous control of hibernation persists in deep hypo- thermia as evident from °c the sensitivity to thermal % and other stimuli. The arousal from hibernation is equally an active pro- % cess, very efficiently con- trolled, so that organism \ l o6, can produce a great x0! i . eels, amount of heat in mini- ® intact mum of time. The coordi- nation of thermogenetic 2% ‘nae ey a processes depends also on eae a ae the activity of nervous centres. Characteristic of Fig. 6. Changes in body temperature of the bat Myotis myotis awakening is the prepon- during entering hibernation (Jansky, HAJexk, 1961) derence of sympathetic nervous system, leading to vasoconstriction and to an increase in heart rate. The main source of heat in awakening is again constituted by shivering. However, nonshivering heat production was also found during arousal and also the rapidly beating heart, working against a high pressure, may contribute a certain amount of heat. Summary On the basis of all mentioned data we conclude that the adaptations of temperature regula- tion to cold may be realized either by an increased ability to produce heat or by reducing the heat loss. While the individual adaptations are manifested chiefly metabolically as evident from an increased capacity of heat production, the inherited adaptations are realized mainly by mechanisms leading to the heat loss reduction (e. g. increased insulation by fur or by superficial hypothermia, reduction of body surface area, active choice of environmental tem- perature and lowering the body temperature). The control of the mentioned adjustments con- sists in the changes in function of the central and sympathetic nervous systems inducing changes in intensity of the energy metabolism (individual adaptations), changes in the plasti- city of vasomotor mechanisms and in heat production of hibernators during entering into and awakening from hibernation (evolutionary adaptations). Morphologically based adjust- ments (improvement of insulation by fur) appearing in both evolutionary and individual adaptations forms the connecting link between both types of adaptations. Zusammenfassung Aus allen erwahnten Daten folgern wir, daf§ die Adaptationen der Temperaturregulierung bei Kalte entweder durch die erhdhte Warmeproduktion oder durch die Verringerung des Warmeverlustes erreicht werden. Wahrend die individuellen Adaptationen hauptsachlich meta- bolischer Art sind, was durch die erhéhte Kapazitat der Warmeproduktion in Erscheinung tritt, findet man erbliche Adaptationen zumeist in Form von Mechanismen, die eine Verringerung des Warmeverlustes bewirken (z. B. erhdhte Isolierung durch das Fell oder durch oberflachliche 518 172 L. Jansky Hypothermie, Verringerung der Korperoberflache, aktive Wahl der Umgebungstemperatur und Absinken der K6rpertemperatur). Die Steuerung der erwahnten Anpassungen beruht auf Veranderungen in der Funktion des zentralen und des sympathischen Nervensystems, welche Veranderungen in der Intensitat des Energiestoffwechsels (individuelle Adaptationen) hervor- rufen, weiterhin Veranderungen in der Plastizitat der vasomotorischen Mechanismen und in der Warmeproduktion von Winterschlafern beim Einritt in den Winterschlaf und beim Erwachen (evolutive Adaptationen). Morphologische Adaptationen (Verbesserung der Isolierung durch das Fell), die sowohl als evolutive und auch als individuelle Adaptationen vorkommen, stellen die Verbindung zwischen beiden Typen der Adaptation her. Literature Hart, J. R. (1956): Seasonal changes in insulation of the fur. Can. J. Zool. 34: 53—57. — (1963a): Surface cooling versus metabolic response to cold. Fed. Proc. 22: 940—943. — (1963b): Physiological responses to cold in nonhibernating homeotherms. Temperature — Its Measurements and Control in Science and Industry 3: 373—406. Hart, J. S., and Jansxy, L. (1963): Thermogenesis due to exercise and cold in warm and cold acclimated rats. Can. J. Biochem. Physiol. 41: 629—634. Hsien, A. C. L., and Cartson, L. D. (1957): Role of adrenaline and noradrenaline in chemical regulation of heat production. Amer. J. Physiol. 190: 243—246. IrvinG, L. (1956): Physiological insulation of swine as bare-skinned mammals. J. Appl. Phy- siol. 9: 414—420. ; Jansxky, L. (1965): Adaptability of heat production mechanisms in homeotherms. Acta Univ. Carol.-Biol. 1—91. Jansky, L., and Hajek, I. (1961): Thermogenesis of the bat Myotis myotis Borkh. Physiol. Bohemosloy. 10: 283—289. Jansky, L., and HanAk, V. (1959): Studien tiber Kleinséugerpopulationen in Siidbdhmen. II. Aktivitat der Spitzmause unter natiirlichen Bedingungen. Saugetierkundliche Mitteilungen 8: 55—63. Lyman, C. P. (1963): Homeostasis in Hibernation. Temperature — Its Measurement and Control in Science and Industry 3: 453—457. SCHOLANDER, P. F., Hock, R., WaLTERs, V., JOHNSON, F., and Irvine, L. (1950a): Heat regu- lation in some arctic and tropical mammals and birds. Biol. Bull. 99: 237—271. SCHOLANDER, P. F., Watters, V., Hock, R., and Irvine, L. (1950b): Body insulation of some arctic and tropical mammals and birds. Biol. Bull. 99: 225—236. Author’s address: L. Jansky, Ph. D., Department of Comparative Physiology, Charles Uni- versity, Prague 2, Vini¢éna 7, CSSR 519 Ecology (1974) 55: pp. 412-419 BAT ACTIVITY AND POLLINATION OF BAUHINIA PAULETIA: PLANT-POLLINATOR COEVOLUTION' E. RAYMOND HEITHAUS" Department of Biological Sciences, Stanford University, Stanford, California 94305 PAUL A. OPLER Organization for Tropical Studies, Apartado 16, Ciudad Universitaria, Costa Rica, Central America HERBERT G. BAKER Department of Botany, University of California, Berkeley, California 94720 Abstract. The relationship between the pollination biology of a tropical plant, Bauhinia pauletia, and the foraging strategies of the nectarivorous bats visiting it was studied. At least two bat species are pollen vectors, Phyllostomus discolor and Glossophaga soricina. Artibeus jamaicensis and Sturnira lilium were also captured near Bauhinia flowers. Larger bats (P. discolor) drain flowers of nectar and forage in groups, while smaller bats (G. soricina) make brief visits and forage independently. These foraging strategies should optimize energetic gain for the bats and promote outcrossing for the plant. Bauhinia pauletia is self-compatible, but is found where conditions favor outcrossing. Andromonoecism (the presence of hermaphrodite and male flowers) in this species appears to be an adaptation to pollination by large pollinators that also promotes outcrossing. Key words: Andromonocecism, pollination. INTRODUCTION Bats are important pollinators in tropical commu- nities, with at least 500 species of neotropical plants wholly or partly dependent on bats for pollination (Vogel 1969). Most of the literature on this subject has been devoted to describing instances of bat pollination and summarizing floral characteristics conducive to chiropterophily (Faegri and van der Pijl 1966). Some effort has gone into analysis of pollen feeding of glossophagine bats (Alvarez and Quintero 1969, Howell 1972). The importance of bats as pollinators goes beyond the large number of species involved. Janzen (1970) has argued that the evolutionary plasticity afforded by outcrossing is extremely important in tropical communities, and Bawa (in press) found a high proportion of genetically self-incompatable tree spe- cies in one dry, lowland, tropical community. Others claim that wet tropical forest trees ought to be capable of inbreeding because of the large distances between trees (Baker 1955, Federov 1966), but such widely dispersed plants could be outcrossed if bats act as long-distance pollen vectors (Baker 1973). The effectiveness of bats in outcrossing depends both on plant flowering strategies and the foraging patterns of bats. This paper studies one species of chiropterophilous plant and the foraging patterns of 2 Manuscript received February 10, 1973; accepted July Paje, MOYI Bs * Current address: Department of Biological Sciences, Northwestern University, Evanston, Illinois 60201. behavior, Bauhinia, Chiroptera, coevolution, energetics; the bats visiting it, in the Tropical Dry Forest life zone (Holdridge 1967) in Costa Rica. Bauhinia pauletia Pers. (Caesalpiniaceae) is found from southern Mexico to Trinidad. In Costa Rica it is uncommon in the Pacific lowlands, occurring in distinct small patches in savanna or pasture habi- tats (Standley 1937), while elsewhere it occurs in sparse to moderate stands (Wunderline, pers. comm.). METHODS Floral biology This study was conducted 1.5 km west of Canas, Guanacaste Province, Costa Rica. A 100 by 15 m patch of Bauhinia pauletia containing more than 20 individuals was observed casually in December 1970 and intensively from October 11, 1971, to January eos Two types of flowers may be found on individual shrubs, hermaphroditic and functionally staminate with an aborted gynoecium (i.e., plants are andro- monoecius). The flowers are borne on a woody inflorescence that retains floral scars after unfer- tilized flowers fall off. Flowers were observed in situ to determine the time of opening and anthesis and the pattern of nec- tar production. The relative frequency of staminate and hermaphroditic flowers was determined for 10 nights, distributed from October 16 to December 12, by counting flowers along a transect. The reproduc- tive success of 81 marked inflorescences was followed by comparing the number of floral scars to the 520 Early Spring 1974 number of fruits produced and multiplying by the percent of the flowers that set pods when hand- pollinated. These inflorescences were observed at 10- to 12-day intervals, October 15—December 12 to determine the rate of flower production and the re- productive success through time. Breeding system studies of Bauhinia pauletia were conducted on November 20 and December 2. Buds were opened by hand at 1700 hr, anthers of her- maphroditic flowers were removed, and paper bags were placed over the flowers. Between 1900 and 2030 hr, the treated flowers were self-pollinated, cross-pollinated, or rebagged without further treat- ment. Twenty to 25 flowers distributed over several individuals were used for each treatment. Treated inflorescences were checked after 10 to 20 days to determine the extent of fruit set. Plant voucher specimens were collected and de- posited at the Missouri Botanical Garden, St. Louis, Missouri; Field Museum of Natural History, Chi- cago, Illinois: and Universidad de Costa Rica, San Jose, Costa Rica. Pollinator activity The behavior of flower visitors was studied by direct observation and photography. Bats were cap- tured with nylon mist nets set near the shrubs on October 11 and 16, and November 16. Bats were tested for the presence of pollen, identified, banded with numbered aluminum bands, and released. Pollen loads were sampled by rubbing captured bats with a glycerin jelly preparation that was later mounted on glass slides as described by Beattie (1971). Pollen was identified by comparison with known types of pollen collected in Guanacaste. Visual observations were made on November 4 and 5 between 1830 and 2130 hr to ascertain whether visitation rates varied with time, position of the flower, or type of bat. On November 4, three ob- servers watched. different sections of the patch con- taining several shrubs and 30-60 open flowers. Visitation times to the nearest 10 min and the size of the bat visitor (“large vs. ‘“small”) were re- corded. Observations were made by moonlight when possible or with the aid of dim flashlights. Six observers repeated visual observations on November 5, from 1810 to 2125 hr. Each person recorded visits in a 17 m section of the patch con- taining roughly 40 to 70 flowers. The following information was recorded for each visit: size of the bat, relative flower position (top of canopy vs. low in canopy), and time of the visit to the nearest 5 min. Since bat activity might be influenced by lunar cycles, stigmas were examined for pollen deposition 52.1 BAT POLLINATION OF BAUHINIA PAULETIA 413 on two mornings, once after a full moon and once after a new moon (December 3 and 17). Twenty- six and 11 stigmas respectively were examined, and the number of pollen grains touching the receptive portion of each stigma was counted. RESULTS Bauhinia pauletia flowers opened nearly synchro- nously between 1815 and 1900 hr and were receptive for only one night. Individual flowers usually opened in less than 5 sec and some pollen was immediately available. Each inflorescence produced a pair of flowers every 2nd or 3rd day, with a mean interval between successive antheses of 2.7 days (N = 489, SD i= 576)F Only five of the 10 stamens in a flower produced pollen. The remaining five stamens were atrophied and lacked productive anthers. Anther dehiscence began in the bud at 1800 hr, but pollen was not fully exposed until approximately 30 min after open- ing. Anthers were loosely attached to the stamens and often were detached during the night by polli- nator activity or the wind. Little pollen was avail- able by 0500 hr on the morning following opening. Nectar flow began just before flower opening and continued at an approximate rate of 0.5 ml/hr for the first several hours. No measurements were made between 2330 and 0500 hr. Nectar accumulated in the calyx, and small amounts moved up the basal portion of the stamen filaments by capillary action. All flowers began to droop and wilt the morning following anthesis, and those which had not been pollinated dropped after | to 3 days. Pollinated flowers remained and incipient pod formation could be noted a few days following pollination. Flowers were either hermaphroditic or functionally staminate. Each night 25% to 60% of the flowers contained degenerate pistils that dropped from the flower at anthesis. On any particular night, a single plant produced predominantly one type: however, a pair of flowers on one inflorescence sometimes in- cluded both types. Individuals were not always con- sistent from night to night in the production of one or the other flower type. The rate of flower pro- duction and the percentage of hermaphroditic flowers on 10 nights covering a 2-mo period is shown in Fig. 1. increased from October 16 to November 4, then de- The proportion of hermaphroditic flowers creased through the rest of the flowering period. The small increase seen on December 12 was not significant (proportionality test). The initial, highest, and lowest values, however, are significantly different from each other (proportionality test, P > .95). The mean percentage of hermaphroditic flowers for all nights was 42.0% (N = 869). 100 o © oOo % NUMBER OF FLOWERS DILIGOYHdVWY 3H 5 19 3 7 31 14 28 12 SEPT OcT NOV DEC DATE Fic. 1. The rate of flower production of 81 inflores- cences and the proportion of hermaphroditic flowers produced in a patch of Bauhinia pauletia near Cajas, Costa Rica. Solid line = No. of flowers. Dashed line = % of hermaphroditic flowers. The rate of flower production was greatest during October, then gradually declined (Fig. |). The results of the breeding system experiments are summarized in Table |. All treatments resulted in some fruit set, with cross-pollinated flowers having the same success as selfed flowers and with control flowers showing the least success. The difference between fruit set in the self-pollinated group and the cross-pollinated group was not significant (y° = 0.824, df = 1). The fruit set of control flowers was significantly lower than that of selfed flowers (y? = 5.017). These data are based on observations of pod development 10 days after treatment. Wind and animal damage to treated flowers precluded follow- ing development of pods to maturity. Pod develop- ment was initiated by 58.8% of the artificially pol- linated flowers. Mature pods were produced by 12.0% of the 2373 70 ep) i) r in ey HERMAPHRODITIC Oo Zz So z ~ =. . 2 40 \ - . A | 2 sot ere ; : S / \ a \ ‘ i Na ae 6 Al» ive é = x se 10 OF i9 26 > 10 i724 31 immal4 2 28 3 1o SEPT ocT NOV DEC DATE Fic. 2. The proportion of flowers producing pods through time. Solid line = % of all flowers forming pods. Dashed line = % of estimated No. of her- maphroditic flowers forming pods. E.R. SHELPHAUS; «PA; OPLERVAND!H: 1G: BAKER Ecology, Vol. 55, No. 2 TABLE 1. Breeding system experiments Treatment N Pods set % Success Cross 21 14 66.7 Self 30 16 53.4 Control 19 4 21.1 flowers that were observed but not treated. These flowers represent the output of 81 inflorescences over a 3'2-mo period: however, single inflorescences produced flowers for several weeks only. Since only 43.3% of the flowers were estimated to be her- maphroditic and thus capable of producing fruits, pollination success can only be expressed by fruit set success for potentially reproductive flowers. Since 27.8% of the hermaphroditic flowers produced pods, the proportion of untreated flowers producing pods was roughly half the proportion (58.8%) of arti- ficially pollinated flowers that showed incipient pod development. All observed ripe pods contained ma- ture seeds, although these were often destroyed by insects (Bruchidae). The temporal pattern of pod formation for all tlowers on the monitored inflorescences is shown by Fig. 2. The estimated success of hermaphroditic flowers, based on the estimated proportion of her- maphroditic flowers and assuming a constant fertility rate of 58.8% is also shown. Fruiting success ap- pears to be high initially, to decrease, then to increase somewhat at the end of the flowering period. Esti- mates of pollination success for the period prior to October 11 are based on extrapolation of known flowering rates. The pitfalls of extrapolation are acknowledged, but we feel it is justified by the consistent rates of flower production by individual inflorescences that we observed. Many animals were attracted to Bauhinia pauletia flowers soon after anthesis, including small numbers of moths (Noctuidae, Pyralidae, and Sphingidae) and many leaf-nosed bats (Phyllostomatidae). Ob- servations and photographs indicated that noctuids and pyralids withdrew nectar from the flowers while clinging to the calyx (Fig. 4A) and seldom contacted the stamens or pistil. Sphingids were potential pol- linators but few were present. They contacted the floral reproductive parts, but we saw no more than one or two visits per night of observation. However, bats were commonly seen visiting flowers: some bees were observed collecting pollen early in the morning. Sixty-seven bats were captured in mist nets near B. pauletia, 66 of them in 24 net-hours during Oc- tober. Three subfamilies of Phyllostomatidae were represented: Phyllostomatinae: color Wagner, N = 40; Glossophaginae: Glossophaga soricina Pallas, N = 13; and Stenoderminae: Artibeus Phyllostomus dis- 522 Early Spring 1974 BAT POLLINATION OF BAUHINIA PAULETIA 415 TABLE 2. Pollen load type 7 Pollen load type Bauhinia Unknown 23 Bat Bauhinia Crescentia Crescentia Bauhinia Zero Phyllostomus discolor 10 1 7 0 0 Glossophaga soricina 0 3 7 1 1 Artibeus jamaicensis 2 0 0 0 4 Sturnira lilium 1 0 0 0 0 Uroderma bilobatum 0) 0 0 0) 1 jamaicensis Leach, N = 8; Sturnira lilium E. Geof- froy, N = S; and Uroderma bilobatum Peters, N = 1. We banded 41 bats on October 11, and 26 on Oc- tober 16. Only one of these, a male P. discolor, was recaptured near B. pauletia (five nights after banding). The distribution of pollen among the bat species is summarized in Table 2. On 32 of 48 bats tested (84.2%) large amounts of pollen (“pollen loads”) adhered to the wings, head, and body. Phyllostomus discolor and G. soricina carried pollen most fre- quently (91% of 32 pollen loads were carried by these species). Pollen grains from both B. pauletia and Crescentia spp. (Bignoniaceae) were abundant, while one unidentified type was also present. Both Crescentia alata HBK and Crescentia cujete L. were in flower nearby, but their pollen was indistinguish- able. Mixed Bauhinia and Crescentia pollen loads were common, especially on G. soricina. Phyllosto- mous discolor carried Crescentia pollen only in mixed species pollen loads, and even then Crescentia was uncommon relative to Bauhinia pollen. In contrast, G. soricina often carried Crescentia and Bauhinia pollen in equal amounts, so this species appeared to visit Crescentia flowers more often than P. discolor. The capture and pollen load data indicate that P. discolor and G. soricina were the principal bat visitors to B. pauletia. This is supported by photographs of bats approaching or feeding at flowers. It was pos- sible to identify bats on the basis of size, shape of the head, form of the flight membranes, and color in 30 photographs. Phyllostomus discolor (Fig. 5B and 5C) was identified in 13 pictures and G. soricina (Fig. 5D) in 17. No other species could be identified. On November 4 and 5 during 27 man-hours of ob- servation 1147 visits to flowers by bats were re- corded. It was possible to distinguish bats of two sizes, large and small. The four common bat species netted near the flowers were also clearly large or small. Their forearm lengths are an index of differ- ences in total sizes: P. discolor = 59.2-63.2 mm: A. jamaicensis = 54.9-60.6 mm; G. soricina = 33.1— 39.1 mm; and S. lilium = 40.5-43.6 mm (Goodwin and Greenhall 1961). Most visits were made by large bats on both nights (Table 3). The ratio of 4:1 (large:small) in observed visits is close to the ratio obtained from netting results for P. discolor and G._ soricina (Gila e We noted a number of other differences between large and small bats in addition to frequency of visits. These included variations in the floral visita- tion behavior, movement patterns within the plant vicinity, and height of flowers visited. Large bats (924 observations, 9 photographs) invariably grasped a section of branch beneath an open flower with their feet, then bent their heads into the calyx. The wings were usually spread and not used for sup- port. The bat’s weight bent the thin branches so that nectar was drained from the inverted flowers. Visits lasted 1-3 seconds (Fig. 4C and 4D). Small bats, on the other hand, generally hovered in front of a flower and appeared to lap the nectar (Fig. 4D). Such visits lasted less than 1 sec. Small bats sometimes clung to flowers with their thumbs and feet, but flowers were not inverted by their weight. The duration of this clinging visit was also very short, less than 1 sec. The hovering visit was much more common, in a ratio of 12:1 based on 13 photographs. Flowers visited once by small bats were very likely to be visited several more times. For example, one flower was visited 14 times in 30 min. Since the bat that was visiting this flower approached from the same direction and angle each time, the impres- sion created was that the same bat was making re- peated visits. Observations revealed that large bats are most prone to visit flowers classed as “high” in the canopy. Of 924 visits, 87.6% were to high flowers and the TABLE 3. Ratio of large and small bat visits Nov. 4 Nov. 5 % N % N Large 80.1 219 80.5 705 Small 19.9 52 19.5 i7fat 523 416 TABLE 4. Patterns of visitation for large bats Mean Range SD N No. of visits per peak* 14.63 2-61 13-57 49 Duration of peaks (min ) 10.9 5-25 5.83 49 Interval between peaks (min) 21.6 10-55 10.78 43 No. of peaks per section 8:2 7-9 (28 6 E. R. HEITHAUS, P. A. OPLER AND H. G. BAKER Ecology, Vol. 55, No. 2 wm 24 FE ® 20 > a 16 fo} 12 a 8 8 A AY 7 3 vi : * ae LZ SE onerontiads 1900 2000 2100 TIME Fic. 3. The distribution of visits by large bats to _* Peak = any concentration of visits of which at least three occur within one 5-min interval. remainder to “low” flowers. Small bats visited 59.7% high flowers and 40.3% low flowers in 223 visits. Both types of bat visited higher flowers more often (x7. P > .99), but large bats visited the high flowers almost to the exclusion of low flowers. It appeared that the large bats visited inflorescences that would not drop into foliage during their visits. Social behavior during foraging also differed for large and small bats. Large bats appeared to arrive in groups to feed. Groups of two to six bats were often seen flying in a linear formation over the flowers. Vocalizations were commonly heard as these groups flew by. While it was impossible to count all bats feeding in an area at any given time, we estimated that groups consisted of from two to 12 individuals. In contrast, small bats appeared to forage alone. The pattern of visitation to flowers in restricted sectors of the Bauhinia patch supports the hypothesis that large bats feed in groups. The pulsed nature of visits was striking (Fig. 3). After a period of active flower visitation in one section, very few or no visits were likely for up to 55 min (average interval be- tween peak visitation periods = 21.6 min, N = 43). The average period of active visitation was 10.9 min (N = 49), consisting of an average of 14.4 visits. An average of 8.2 periods (range = 7-9) of active visitation were observed in each of the six sections observed for 3 hr on November 5. These patterns are summarized in Table 4. The distribution of TABLE 5S. 40-70 B. pauletia flowers, November 5. flower visits by large bats through the evening is exemplified by Fig. 3 (from Observer 2, November 5). Note that activity reached a peak late in the evening, but that the visits were pulsed throughout the observation period. Observations on November 4 gave similar results, but the data were not lumped with those of Novem- ber 5 because a different time interval was used. The pulsed visitation pattern was generally the same, and there were five to seven visitation periods ob- served. No such patterns were discerned for small bats. Repeated visits in particular sectors were usually to the same flower and seemed to be by the same bat. No groups of small bats were ever seen flying over the flowers. Finally, analyses of pollen loads suggested another difference in visitation patterns. Glossophaga soricina (a small bat) carried Bauhinia pauletia pollen only in mixed pollen loads with Crescentia pollen. Small bats carried either pure or mixed Crescentia pollen. Phyllostomus discolor (a large bat) had pure B. pauletia pollen loads on 55% (10) of the bats tested, and on only 41% (7) were very small amounts (< 5% of all pollen) of Crescentia pollen found. The differences in the flower-visiting behavior between large and small bats are summarized in Table 5. The bat activity level around B. pauletia varied considerably on different nights. This is reflected by the low netting success of November 16 com- Patterns of visitation to Bauhinia pauletia by large and small bats Large Small (Probably Phyllostomus discolor) Visits high flowers Grasps branch beneath flower, pulling it down Drains nectar well Visits in groups in pulses Visits same flower infrequently Carries 55% pure Bauhinia pollen loads; 45% mixed pollen loads (all mixed loads > 90% Bauhinia) (Probably Glossophaga soricina ) Visits high and low flowers Hovers Laps small amounts of nectar Visits singly, flies independently Returns to same flower at short intervals Carries no pure Bauhinia pollen loads; 100% Crescentia or mixed loads 524 Early Spring 1974 Fic. 4. Bauhinia pauletia flower visitors. soricina hovering while feeding. discolor hanging while feeding. pared to October 11 and 16. Differences in moon- light may have influenced activity (Crespo et al. 1972). For example, bat activity during 20 min of observation on December 2 (full moon), but was estimated to be light to moderate on December 16 (new moon). Apparent differences in bat activity during these nights were reflected in the amounts of pollen deposited on stigmas. The mean number of grains adhering to the stigmatic surfaces of pistils collected on December 3 was 23.2 (N = 26, SD = 42.22), while on December 17 the avearge number of grains per stigma was 294 (N = 11, SD = 152.4). This difference was highly significant (y°, P > .99). was nearly absent DISCUSSION AND CONCLUSIONS This study reveals that coevolution between plants and pollinators can be more complex than the ex- change of food for pollinator services. Bats not only effect pollination, they also promote outcrossing in B. pauletia as discussed later. Furthermore, two dis- BAT POLLINATION OF BAUHINIA PAULETIA (A) Noctuid moth approaching base of flower. (C) Phyllostomus discolor reaching for branch below a flower. 417 (B) Glossophaga (D) Phyllostomus tinct floral resource utilization strategies are seen in bats, and these strategies may be related to their evolution of social behavior. Breeding systems which promote outcrossing allow for greater evolutionary plasticity than inbreeding systems (Stebbins 1970). It has been suggested that genetic variability is important to plants subjected to changing selective pressures such as herbivores or seed predators that are also evolving (Janzen 1970). Plant breeding systems in the tropical dry forest region are typified by the prevalence of self- incompatibility systems among trees (Bawa in press), a large number of (Bawa and Opler pers. comm.), and the frequent occurrence of dioecious species other strategies that promote outcrossing (e.g., het- erostyly, protandry). This supports the hypothesis that maintenance of plasticity is generally important there. Bauhinia pauletia is not a likely exception to this generality. As extensive insect damage to seeds was observed, B. pauletia appears to be subjected to the type of changing selection discussed by Janzen 525 418 (1970). Also, the sympatric bat-pollinated B. un- gulata ensures outcrossing through genetic selt- incompatibility (Bawa pers. comm.). Although B. pauletia is genetically self-compatible, self-pollination (autogamy) of flowers is improbable. The apparent correlation between pollen deposition on stigmata and bat activity (on two nights in De- cember) suggests that pollen movement depends greatly on animal transport. The strategy of andro- monoecism seems also to be associated with depen- dence on animal transport of pollen. Self-pollination of flowers during a bat visit is improbable, since bats tend to push the stamens and pistil apart (Fig. 4B- 4D) so anthers are unlikely to contact the stigma. Although small bats tended to visit particular flowers repeatedly, mixed pollen loads on G. soricina suggest that these small bats fly from flower to flower in a “trapline.” Probably these bats visit a series of flowers repeatedly, and their visits decrease the probability of autogamy. The movement of groups of large bats from one area to another clearly pro- motes outcrossing. Pollen transfer among tlowers of the same plant (geitonogamy) is not precluded by bat behavior, but it is clear that bats cause much if not most crossing. The simultaneous production of male and_her- maphrodite flowers on the same individual (andro- monoecism) is rare, and its significance has not been investigated adequately. Carr et al. (1971) report andromonoecism in Eucalyptus spp. of the series Corymbosae but make no attempt to relate the phenomenon to pollination systems. It clearly re- duces inbreeding, since functionally male flowers cannot be self-pollinated. We feel andromonoecism has additional adaptive value because it increases the ratio between pollen and ovules (or pollen and stig- matic surface). Large quantities of pollen may be necessary to ensure deposition of sufficient pollen to fertilize up to 30 ovules per stigma, especially since pollen is scattered over the entire ventral sur- face of bats. The stigmatic surface area is .0O8 cm, while the ventral surface area of just the wings of an average glossophagine bat is 144 cm? (Findley et al. 1972). This means the ratio of wing area (of an average small bat) to stigma surface area is 18,000:1. The need for large amounts of pollen in this system are obvious. Andromonoecism, therefore, may be associated with specialization for pollination by pollen vectors that are very large relative to stigma size. The problem of utilization of large pollen vectors has been solved by other bat-pollinated plants in three basic ways. For example, Pseudobombax bar- rigon (Bignoniaceae) also maintains a high ratio of pollen to stigma area, but by producing hundreds of stamens per flower. Pollen may also be placed on a E.R, HEIDHAUS, PR. Ay OPRLER AND HG: BAKER Ecology, Vol. 55, No. 2 bat selectively as in Bauhinia ungulata, which de- posits pollen primarily on a bat’s abdomen. Finally, larger stigmata, such as found in Ochroma_ pyra- midale (Con. ex Lam.) Urban (Bombaceae), can greatly reduce the relative difference between polli- nator and stigma-surface areas. This explanation of andromonoecism can be ex- tended to other pollination systems. Aesculus cali- fornica (Spach) Nutt. (Hippocastanaceae) is pollinated by butterflies, but it has a minute stigmatic surface (Benseler 1968). The stigmas of eucalypts are also very small, especially relative to the large number of ovules per flower. Bauhinia pauletia nectar is used by at least two species of bats that have evolved different resource utilization strategies. Circumstantial evidence sug- gests that the great majority of the large bats were Phyllostomus discolor, while small bats were Glosso- phaga soricina. Artibeus jamaicensis and Sturnira lilium, characterized by reduced uropatagia easily distinguished in most photographs, were not seen. In addition, fewer than one-third of the captured A. jamaicensis carried pollen. Since we found that A. jamaicensis and S. lilium visited other flowers in the study region, we cannot assume that they never visited B. pauletia: however, they are certainly less important to B. pauletia pollination than P. discolor and G. soricina. Resource utilization patterns appear to be related to aspects of the social behavior of these bats. Visita- tion by P. discolor is clearly coordinated, as indi- cated by the pulsed pattern illustrated in Fig. 4. This pattern and the formation of bats flying over the plants suggests a social organization that includes feeding groups. If so, more than one group was in- volved on November 4 and 5, as observers at op- posite ends of the B. pauletia patch simultaneously watched peaks of visitation on 14 occasions. There- fore, it is impossible to speculate on the cohesiveness of these assemblages. Group foraging by Phyllos- tomus hastatus (Goodwin and Greenhall 1961) and Myotis adversus (Dwyer 1970) has been observed. As Artibeus jamaicensis and Carollia_ perspicillata may also forage in groups, this strategy may be more widespread than previously thought. In contrast, G. soricina forages singly around Bauhinia pauletia. Energetic considerations are of extreme importance in plant-pollinator relationships (Heinrich and Raven 1972, Wolf et al. 1972) and may account for these bat foraging differences. Since the large bat P. dis- color always drains nectar from B. pauletia flowers, the reward in nectar in successive visits is correlated with the time between visits. Short times between repeated visits to the same flower will net the visitor little nectar. By visiting flowers in groups P. discolor may decrease the probability of quick successive 526 Early Spring 1974 visits to the same flower. Furthermore, bats might learn to allow the optimal time between visits to the same group of flowers for sufficient replenish- ment of nectar and to return before competing groups discover the new resource. In contrast, individuals of the smaller bats spend a very short time at each flower, probably lapping small amounts of nectar at each visit. With the slow depletion of nectar, repeated visits to the same flower are not energetically disadvantageous. In fact, there may be some advantage to learning the position of particular flowers and then repeatedly utilizing these sources, because search time would decrease relative to feeding time. Independent foraging appears to be favored when nectar is not drained with each visit. These bat-foraging strategies may parallel finch- foraging strategies in deserts. Cody (1971) found that the formation of foraging flocks of mixed finch species was related to food abundance, the birds forming flocks as food became less abundant. He hypothesized that renewable resources temporarily depleted are most efficiently utilized by flocks that can learn to vary the time between returns to the same feeding points. Phyllostomus discolor foraging may fit this pattern. Independent foraging of finches was observed when resources were abundant. This may be analogous to the independent foraging of G. soricina, which does not immediately deplete the floral nectar supply and thereby has an abundant resource. In summary, Bauhinia pauletia is a genetically selt- compatible plant living in conditions where main- tenance of genetic variability is an asset. Bats pol- linate its flowers and promote outcrossing. Andro- monoecism increases the probability of pollen trans- fer trom these large pollinators to relatively small stigmata and also decreases the probability of au- togamy. Two kinds of bat have evolved different nectar-resource-utilization strategies, but both be- haviors tend to in cross-pollination of B. pauletia flowers. result ACKNOWLEDGMENTS This work was partially financed by OTS Pilot Studies Grant N-70-58, NSF Grants GB-7805 and GB-25592 (Herbert G. Baker and Gordon W. Frankie, Principal Investigators) and a series of NSF grants to Peter H. Raven. We especially thank Patricia A. Heithaus for assistance during this study. Sandra Opler assisted in field observations. John T. Doyen, Theodore H. Fleming, Richard Holm, Peter H. Raven, and an anonymous re- viewer read early drafts and offered many helpful sug- gestions. LITERATURE CITED Alvarez, T., and L. Gonzalez Quintero. 1969. Analisis polinico del contenido gastrico de murciélagos Glosso- BAT POLLINATION OF BAUHINIA PAULETIA 419 phaginae de Mexico. An. Esc. Nac. Cienc. Biol. Mex. 18: 137-165. Baker, H. G. 1955. Self-compatibility and establish- ment after long distance dispersal. Evolution 9: 347— 348. 1973. Evolutionary — relationships between flowering plants and animals in American and African tropical forests, 350 p. /n B. J. Meggers, E. Ayensu, and W. D. Duckworth [eds.] Tropical forest ecosystems in African and South American: a comparative re- view. Smithson. Inst. Press, Wash., D.C. Bawa, K. 1974. Breeding systems of tree species of a lowland tropical community: evolutionary and eco- logical considerations. Evolution. (in press). Beattie, A. J. 1971. A technique for the study of insect-borne pollen. Pan-Pac. Entomol. 47: 82. Benseler, R. W. 1968. Studies in the reproductive biology of Aesculus californicus (Spach.) Nutt. Ph.D. Thesis (Botany), Univ. California, Berkeley. Carn GM. Dad. ‘Carr. and Fay Ross, 197). Male flowers in Eucalypts. Aust. J. Bot. 19: 73-83. Cody, M. L. 1971. Finch flocks in the Mojave Desert. Theor. Pop. Biol. 2: 142-158. Grespo. Ro Es: Be Linhart, Ro Je Bums and Gs C: Mitchell. 1972. Foraging behavior of the common vampire bat related to moonlight. J. Mammal. 53: 366-368. Dwyer, P. D. 1970. Foraging behavior of the Aus- tralian large-footed myotis (Chiroptera). Mammalia 34: 76-80. Faegri, K., and L. van der Pijl. 1966. The principles of pollination ecology. Pergamon Press, New York. 29 ip: Federov, A. A. 1966. The structure of the tropical rainforest and speciation in the tropics. J. Ecol. 54: I-11. Findley. J. S., E. H. Studier, and D. E. Wilson. 1972. Morphological properties of bat wings. J. Mammal. 53: 429-444, Goodwin, G. G., and A. M. Greenhall. of the bats of Trinidad and Tabago. Nat. Hist. 122: 191--301. Heinrich, B., and P. H. Raven. 1972. Energetics and pollination ecology. Sciences 176: 597-602. Holdridge, L. R. 1967. Life zone ecology. Trop. Sci. Cent., San Jose, Costa Rica. 206 p. Howell. D. J. 1972. Physiological adaptations in the syndrome of chiropterophily with emphasis on the bat Leptonycteris Lydekker. Diss. Abstr. Int. B. Sci. Janzen, D. H. 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104: 501- S27); Standley, P. C. 1937. Flora of Costa Rica. Field Mus. Nat. Hist. Publ. Bot. Ser. 18( 1-4). 1616 p. Stebbins, G. L. 1970. Adaptive radiation of repro- ductive characteristics in Angiosperms. I. Pollination mechanisms. Ann. Rev. Ecol. Syst. 1: 307-326. Vogel, Von S. 1969. Chiropterophilie in der neo- tropischen Flora. Neue Mitteilungen III. Flora, Abt. B 158: 289-323. Wolf, L. L., F. R. Hainsworth, and F. G. Stiles. 1972. Energetics of foraging: rate and efficiency of nectar extraction by hummingbirds. Science 176: 1351- 1352: 1961. Review Bull. Am. Mus. 527 ACTA THERIOLOGICA VOL. XIV, 1: 1—9. BIALOWIEZA 5.1V.1969 Michael H. SMITH, Ronald W. BLESSING, James L. CARMON and John B. GENTRY Coat Color and Survival of Displaced Wild and Laboratory Reared Old-iield Mice [With 1 Table and 4 Figures] Wild and laboratory reared mice from central Florida and South Carolina were released into enclosures on the significantly darker South Carolina soils. The lighter southern mice disappeared at the same rate as the darker northern form, as did the males and females from both localities. Prior experience with field conditions was asso- ciated with a large selective advantage; the laboratory reared mice disappeared much faster than the wild mice. The correlation between soil and pelage color implies a selective advantage for mice to match the soil, but this advantage must be relatively small because the light form did not disappear at a higher rate than did the darker mice. The relationship between reflectivity and wavelength was linear for both pelage and soil samples. This probably means that the evolution of the dorsal pelage color in this species takes place by modifications in the slope or the intercept of the pelage line. I. INTRODUCTION The old-field mouse, Peromyscus polionotus Wagner, shows con- siderable morphological variation throughout its range (SG mith, 1966). The adaptive significance of many of these variations has been implied by correlational techniques, but no attempt has been made to experi- mentally determine under field conditions the selection coefficients for any of these traits. Despite a lack of data, it can still be argued that the observed polymorphisms are not random but rather represent evo- lutionary responses to differences in the local environments. Following this reasoning, we would expect mice currently living in one locality to be better adapted for survival in this particular area than mice that are taken another area and released at the first site. Of course, it is necessary to assume that the areas are separated to such an extent 1 528 ) M. H. Smith et al. that genetic exchange between the populations is negligible, the environ- ments at the two sites are significantly different, and finally that the populations have persisted in these areas for a sufficient length of time for selection to produce differences between them. Under these condi- tions, two populations would normally be expected to differ in more than one way. For our purposes in this paper, we will concentrate only on differences in coat color of the old-field mouse in relation to the color of their soil background. II. MATERIALS AND METHODS Old-field mice were captured in the field or reared in the laboratory and then released into two outdoor enclosures. The enclosures, each containing approxi- mately two acres, were adjacent to one another in field 3—412 on the Savannah River Plant in Aiken County, South Carolina, USA. The vegetation in area 3—412 is typical on an old-field (Odum, 1960; Golley & Gentry, 1965), and P. po- lionotus occurs abundantly in this area (Caldwell, 1964; Davenport, 1964). Caldwell & Gentry (1965) described an enclosure similar to the ones used in this study. The wild mice were collected from other fields on the SRP and also from Citra in Marion County, Florida. Laboratory reared mice were taken from two different colonies; one was located at the University of Georgia and the other at the Sa- vannah River Ecology Laboratory (see Carmon, Golley & Williams, 19638, and Smith, 1966 for details concerning the maintenance of the colonies). The University of Georgia colony, which was in its seventh generation in the labor- atory, was derived from a wild stock collected in the 3—412 area. The other colony came from stock collected in the Ocala National Forest just east of Citra, Florida and was in its fifth to seventh generation in the laboratory. The labora- tory animals were from three to six months of age. Each experiment consisted of releasing 10 adult males from each area into one of the enclosures and 10 adult females from each area into the other enclosure. Pregnant females were excluded from all experiments. The wild mice were held in the laboratory for about 10 days before their release. Experiments consisted entirely of wild mice or of laboratory reared mice; the two types were never released in the enclosures at the same time. Two experiments were conducted with laboratory reared mice and two with the wild mice; a total of 160 mice, 80 wild and 80 reared in the laboratory, were released. The order of the experiments was ran- domly selected; it was laboratory, wild, wild, laboratory. Sex, locality, and wild versus laboratory origin were the three factors being tested. The various types of mice were placed into the enclosures in a random order with the restriction that each factor must be tested twice in each enclosure. Each mouse was toe clipped and then released. Populations were censused by live trapping for one day each week for a month. At the end of this time the survivors were removed and another experiment started. The first experiment was started on January 12, 1967 and the last one on May 2, 1967. There were 134 traps per enclosure, and they were distributed in a grid with 30 feet between the traps. 529 Coat color and survival of mice a Reflectance was recorded for the mid-dorsal pelage and for the surface and subsurface soil where the mice were captured. Reflectance was measured be- tween 400 to 700 mu (violet to red) using the Bausch and Lomb Spectronic 505 Recording Spectrophotometer with its visual reflectance attachment in a way similar to the method used by Sealander, Johnston & Hamilton (1964). Flat skins were used in determining the reflectance of the pelage. The mice used in this part of the work were collected at the same time and areas at those released in the enclosures. Soil samples were taken from areas alongside the burrows in which the mice were captured. The reflectance at eight equally spaced points from 400 to 700 mu was used for the statistical analyses. Reflectivity is given as a percentage of the amount of light reflected from a pressed white magnesium carbonate standard. III. RESULTS There was a linear relationship between wavelength (X) and amount of light (Y) reflected from each soil sample or from the pelage of each mouse. Each sample was analyzed separately, so a series of values for Table 1. Results of linear correlation and regression analyses of the relationship between reflectivity and wavelength between 400 to 700 mu for individual soil and pelage samples from Florida and South Carolina. oe FLORIDA SOJL SOUTH CAROLINA SOIL Statistical aus oes Parameters Pelage | Surface | Subsurface | Pelage Surface |Subsurface Sample | Size * | 12 10 10 | 19 15 15 Range of | | | Te | .907—.995 | .992—.998 .9S0—.998 | .968—.990 | .956—.994/} .951—.991 Range of | Gates 4.49—11.94 16.27—20.99 12.66—18.68 | 2.68—8.53 |9.98—14.99| 8.03 —14.88 G22 Sh. Gy (sm wi 17.17.44) 14.12--1.64} 4.36-.37 | 11.41--.32)|° 11:07=-.46 Range of | ton Ne 1.30—2.68 3.71—7.55| 8.43—10.72 | 1.89—5.32 | 3.08—6.87 | 3.35—8.72 bt SP Heel Ome 1.67.01 | 4.61+.03 Groo=t=. 02 2.88-+.02 | 4.63.02 5.48+-.04 | * The number of observations for each regression equals 8, ** All r values were significant at the 0.01 level, *** q is given in per cent reflectivity at 400 mu. the correlation coefficient (7), the intercept (a) and the slope (b) were generated (Table 1). A linear model accounted for the majority of the variability in all cases (82.3 to 99.6%). The pooled data for reflectivity of the pelages and surface soils are given in Figs. 1 and 2, respectively. Surface soils from Florida and South Carolina are obviously different in reflectivity at the various 530 4 M. H. Smith et at. wavelengths but the same is not true for the pelages. However, it would be an error to conclude from Fig. 1 that the relationship between re- flectivity of the pelage and wavelength is necessarily the same in the two areas, since the pooled data consists of a series of independent straight lines. In South Carolina b is larger for a given a than in Flo- rida. In other words, the ratio of reflected red to violet light is larger for a given amount of reflected violet light in South Carolina than in 30 95 PELAGE inet V, ao Florida S | ——— South Caroline = 20 ws) WwW _ re uJ co |§ kK Ze -_ o 10 oc uJ «ole a «co aleehe one |--do> 5 iat : a 0 400 440 480 520 560 600 640 689 WAVELENGTH Fig. 1. The range and mean reflectance values for the mid-dorsal pelage of Peromyscus polionotus from Florida and South Carolina as a function of wave- length from the violet (400 mw) to the red (700 mu) end of the spectrum. Reflec- tance is given as a percentage of the amount of light coming off a pressed white magnesium carbonate standard. Florida. The distribution of the b and a values for the pelages, surface soils, and subsurface soils from South Carolina and Florida is given in Fig. 3. The relationships between b and a differs in each case for the two areas. The disappearance rates of the four groups are given in Fig. 4. There were no significant differences between the disappearance rates of Flo- rida and South Carolina mice (y? = 0.18), or of males and females (y? = 0.18), or in the two enclosures (v2 = 2.2), but wild mice survived better than laboratory reared mice (vy? = 12.84). 531 Coat color and survival of mice 5 IV. DISCUSSION The linear mathematical model accounted for more than 82 per cent of the variability between reflectivity and wavelength for every soil and pelage sample. The similarity of the relationship for the two types of samples was most likely the result of selection for the mice to match their background. Dice (1947) showed that mice that contrast with their background were captured by owls more often than those that blended in with their background. However, the exact way in which 40 SURFACE SOIL. BOSOG Florida —— South Carolina 30 eo --" = = PER CENT REFLECTANCE 400 440 480 520 960 600 640 680 WAVELENGTH Fig. 2. The range and mean reflectance values for dry surface soils from Florida and South Carolina as a function of wavelength from the violet (400 mu) to the red (700 mu) end of the spectrum. Reflectance is given as a percentage of the amount of light coming off a pressed white magnesium carbonate standard. populations respond to selection of this kind was not known. It now appears that there are only two parameters that are subject to modifi- cation by selection. These are the slope (b) and the intercept (a) of the reflectance line. This statement probably has general applicability for many, if not all, species of small mammals; we recently found a signi- ficant linear correlation between reflectivity and wavelength for six species picked at random from the University of Georgia’s museum (manuscript in preparation). 532 6 M. H. Smith et al. The gross similarity of the mathematical relationships goes beyond mere linearity. Slopes and intercepts were positive for all samples. The largest intercepts for the pelage lines were associated with the largest rece aca aeaegeenel mca al cage oa a T Tf faa ae Pameenlarinealy actellpery an) hag s aaa ean laa aT H e é Soil eo °. Oe 1 Horizon e © Location AB Pelage =“ $C. 3-412 ao 4 ° i Al CITRA, Fla. @ @ a ° ° ) 2 ° ° = ° Gi | 4 Sie 5 = a o°Qo 3 Con coo oe 4b P ° on oa z s =I A 4 ° a a. SS pA ets > 1 2 < | [ : 5 “ a a G 4 rear cee es ene | rd | rere | ON ral | Poe | Pw | Ea) ees | deen | ee | eco | ee ee fe Pe 2 3 4 5 6 7 8 9 10 u (2 13 4 18 16 7 18 19 co Oa £1072 Fig. 3. The slope (b) plotted against the intercept (a) of the linear relationship between reflectance and wavelength for pelages, surface soils (A), and subsurface soils (B) from South Carolina and Florida. Percent Survival r) F lorida © South Carolina =a -- Wild — Laboratory | Faas (Seer eens) Ae eee eee eae Dente ae IE eee es Oa | 2 S| 4 Time (weeks) Fig. 4. Disappearance rates of wild and laboratory reared old-field mice from Florida and South Carolina released in South Carolina. intercepts for the soil lines. Despite these similarities there were dif- ferences in the reflectivity of the pelages and soils at the two localities. The differences include the slopes of the pelage and subsurface soil lines and the intercepts of the surface soil lines. Both the mice and the 533 Coat color and survival of mice 7) backgrounds upon which they occur are different in the two areas, and thus there is reason to expect the light Florida mice to disappear faster then the dark South Carolina mice when released on the darker north- ern soils. The Florida and South Carolina mice did not disappear at dif- ferent rates. Since the reason(s) for this contradiction is not readily apparent from the data, it is necessary to examine some of the assump- tions underlying our reasoning concerning differential survival. First, we must assume that there was sufficient selection pressure to cause an Observable difference in the survival rates of the various groups during the study period of one month. The relatively high dis- appearance rate of the laboratory reared mice was probably the result of a high selection pressure. Most of the mice disappear during the first week after introduction, and the survival curves are almost horizontal after this time even for intervals longer than one month (Schnell, 1964; Golley & Gentry, in press). Second, predators must use the visual cues associated with the dorsal pelage to locate the mice. There is no way to test this assumption with the available data. However, considering the relatively high survival rate of the wild mice, it seems unlikely that many of the mice escaped from the enclosures. Thus, their disappearance is probably synonymous with their death by predation or disease. The latter is not probably since none of the mice appeared to be sick when captured in the traps. Potential predators include several species of large mammals, rap- torial birds and snakes. Large snakes do go in and out of the enclosures over the sheet metal fence, and many of these species are known to eat Peromyscus on the Savannah River Plant (Duever, 1967). Since the relative importance of each of the potential predators and of the various senses used in their hunting behavior is not known, it could be con- cluded that the predators of the mice in the enclosures were not using the visual cues associated with the dorsal pelage to locate their prey. This conclusion is inconsistent with the overall correlation between soil and pelage color found in this species by ourselves and Hayne (1950). It seems more likely that there is only a slight selection pressure for modifying the slope and intercept of the reflectivity-wavelength rela- tionship of the dorsal pelage in relation to similar values for the soil. Under these conditions it would take a relatively long period of time to produce the differences in the dorsal pelage that are used to distinguish between the various subspecies (Schwartz, 1954). As the selection coefficient (s) approaches 0, the sample size needed to adequately estimate s approaches infinity. Our sample size was pro- bably too small to detect a slight difference in the survival rates of the mice from the two localities. Prior experience with field conditions was 534 8 M. H. Smith et al. associated with a large selective advantage. Thus learning is apparently very important to the survival of mice under natural conditions. S mat (1967) presented evidence for a different disappearance among the sexes based on sex ratios among young and adult mice, but the difference would have been slight and accordingly undetectable considering our sample size. These data are consistent with the conclusions made above. Acknowledgements: The senior author was supported during the preparation of the manuscript by an Atomic Energy Commission Contract AT(40—1)—2975. La- boratory reared mice from South Carolina were also provided by funds from this grant. Two of the junior authors were supported by an AEC Contract AT(38—1)— 310 while conducting the field work in South Carolina. Both contracts are with the University of Georgia. Travel funds to collect mice in Florida were provided by an NSF Grant GB5140. We would like to thank Drs. R. J. Beyers and J. W. Gibbons for critically reading the manuscript. REFERENCES 1. Caldwell, L. D., 1964: An investigation of competition in natural popula- tions of mice. J. Mammal., 45: 12—30. 2. Caldwell, L. D. & Gentry, J. B., 1965: Interactions of Peromyscus and Mus in a one-acre field enclosure. Ecology, 46: 189—192. 2, Carmon, J. L, Golley, Fr. B.& Williams, RK, G. 1963: An analysis of the growth and variability in Peromyscus polionotus. Growth, 27: 247—254. 4. Davenport, L. B, Jr., 1964: Structure of two Peromyscus polionotus po- pulations in old-field ecosystems at the AEC Savannah River Plant. J. Mam- mal., 45: 95—113. 5. Duever, A. J., 1967: Trophic dynamics of reptiles, in terms of the com- munity food web and energy intake. M. S. thesis, Univ. Georgia, 89 p. 6. Dice, L. R., 1947: Effectiveness of selection by owls of deer mice which con- trast in color with their background. Contrib. Lab. Vert. Biol. Univ. Mich., 34: 1—20. 7. Golley, F. B. & Gentry, J. B., 1965: A comparison of variety and stand- ing crop of vegetation on a one year and a twelve year abandoned field. Oikos, 15, 2: 185—199. 8. Golley, F. B.: Response of rodents to acute gamma radiation under field conditions. Proc. Sec. Nat. Symp. Radioecology, Ann Arbor, Mich. [in press]. 9. Hayne, D., 1950: Reliability of laboratory-bred stocks as samples of wild populations, as shown in a study of variation of Peromyscus polionotus in parts of Florida and Alabama. Contrib. Lab. Vert. Biol. Univ. Mich., 46: 1—56. 10. Odum, E. P., 1960: Organic production and turnover in old field succession. Ecology, 41: 34—49. 11. Schnell, J. H., 1964: An experimental study of carrying capacity based on the disappearance rates of cotton rats (Sigmodon hispidus komareki) intro- duced into enclosed areas of natural habitat. Ph. D. diss., Univ. Georgia, 46 p. 12. Schwartz, A., 1954: Old-field mice, Peromyscus polionotus, of South Ca- rolina. J. Mammal., 35: 561—569. 13. Sealander, R. K, Johnston, R. F.. & Hamilton, T. H., 1964: Colo- rimetric methods in ornithology. Condor, 66: 491—495, 535 Ubarwienie futerka a przezywanie Peromyscus polionotus 9 14. Smith, M. H., 1966: The evolutionary significance of certain behavioral, physiological, and morphological adaptations of the old-field mouse, Pero- myscus polionotus. Ph. D. diss., Univ. Florida, 186 p. 15. Smith, M. H., 1967: Sex ratios in laboratory and field populations of the old-field mouse, Peromyscus polionotus. Researches Population Ecology, 9: 108—112. Received, June 8, 1968. Mailing address: Savannah River Ecology Computer Center Department of Zoology and SEG oes University of Georgia Institute of Ecology Aiken, Athens, University of Georgia South Carolina, USA 29801 Georgia, USA 30601 Michael H. SMITH, Ronald W. BLESSING, James L. CARMON i John B. GENTRY UBARWIENIE FUTERKA A PRZEZYWANIE DZIKICH I LABORATORYJNYCH PEROMYSCUS POLIONOTUS Streszezenie Dzikie i hodowane w laboratorium Peromyscus polionotus (Wagner, 1843) byty wpuszczone do zagrod w Potudniowej Karolinie. Chociaz gleby w Karolinie sq ciemniejsze niz na Florydzie (Fig. 2), to jednak kolor futerka badanych po- pulacji myszy nie roznit sie (Fig. 1). Zaleznos¢ pomiedzy zdolnosciq odbijania Swiatia a diugoscia fali bylta liniowa zardwno dla skorek jak i dla prdébek gleby (Tabela 1). Myszy z Florydy wydawaly sie na oko jasniejsze i miaty mniejszy kat nachylenia prostej regresji przy danej state} wielomianu w pordwnaniu do my- szy z Poltudniowej Karoliny (Fig. 3). Naprzekoér tym réznicom, jaSniejsze osobniki ginely w takim samym tempie jak ciemniejsze z poludnia. Dotyczy to zaréwno samcow jak i samic z obu miejscowosci (Fig. 4). Wezegniejsze doswiadczenia w warunkach terenowych byly zwiazane z duzym zréznicowaniem w _ selekcji; ho- dowane w laboratorium myszy ginety znacznie szybciej} w porownaniu z dzikimi (Fig. 4). Korelacja miedzy barwa gleby a barwa futerka zwierzecia sugeruje istnienie selektywnej dominacji myszy przystosowanych do gleby. Dominacja musi byé wzglednie mala, poniewaz jasne formy nie gina w wiekszym stopniu niz ciemne. Ewolucja w ubarwieniu grzbietowej strony futerka u tego gatunku zachodzi prawdopodobnie poprzez modyfikacje kata nachylenia linii obrazujacej zaleznos¢ pomiedzy zdolnoscia odbicia Swiatta od powierzchni futerka a dlugoscia fali lub tez przez zmiane stalej wielomianu rownania regresii. 536 SECTION 6—ZOOGEOGRAPHY AND FAUNAL STUDIES Studies of faunas, both of local areas and of broad regions, have contributed substantially to the literature in mammalogy. From the earliest contributions to the present, papers and books dealing with faunistics have included much information on systematics, ecology, distribution, ethology, and reproduction, among other topics; the sobriquet “natural historian” implied an interest in all these fields and more. Darlington’s Zoogeography (1957) and Udvardy’s Dynamic Zoogeography (1969) are good sources of general information on that subject; Hesse et al. (1937) is a substantial and still useful earlier reference. Insular biogeography was aptly dealt with by Carlquist (1965) and in a more quantitative and theoretical way by MacArthur and Wilson (1967). Other general treatises that should be called to the attention of the beginning student include Matthew's (1939) Climate and Evolution and Dice’s (1952) Natural Communities. Among the major faunal catalogues are Allen (1939) for Africa, Ellerman and Morrison-Scott (1951) for the Palearctic, Miller and Kellogg (1955) and Hall and Kelson (1959) for North America, Cabrera (1958, 1961) for South America, and Troughton (1965) and Ride (1970) for Australia. At the re- gional level, recent treatments of the faunas of the whole of Canada (Ban- feld, 1974) and the eastern half (Peterson, 1966), the East African countries of Kenya, Tanzania, and Uganda (Kingdon, 1971, and subsequent volumes), West Africa (Rosevear, 1965, 1969), Rhodesia, Zambia, Malawi and Botswana (Smithers, 1966, 1971), the Soviet Union (Ogney, 1962, and subsequent vol- umes), China and Mongolia (Allen, 1938, 1940), Arabia (Harrison, 1964, and subsequent volumes ), are excellent examples, as are many of the state lists pub- lished for North America (for example, Hall, 1946; Jackson, 1961; Baker and Greer, 1962; Jones, 1964; Anderson, 1972; Armstrong, 1972; Lowery, 1974; Bowles, 1975; Findley et al., 1975). Hall’s Mammals of Nevada stands out in completeness from most points of view, whereas Armstrong’s study of mammals in Colorado is especially good with respect to zoogeographic analyses and Lowery’s book on Louisiana is particularly appealing to the specialist and nonspecialist alike. In terms of smaller geographic areas, Harper (1927) on the Okefinokee Swamp, Johnson et al. (1948) on the Providence Mountains of California, Anderson (1961) on the Mesa Verde of Colorado, Foster’s (1965) study of the Queen Charlotte Islands, and Turner’s (1974) paper on the Black Hills illustrate that substantial information can be gleaned from the study of a geographically restricted fauna. These publications as well as several repro- duced here clearly indicate that the serious student of faunistics must be broadly trained in the discipline of mammalogy. Because of interest in faunal studies over the years, it was inevitable that certain “laws”—directed at overall explanations for natural phenomena asso- ciated with distribution and variation—would emerge. These have been of two basic sorts, various “ecological rules” such as those proposed by Allen, Bergmann, and Gloger, and the biogeographic systems proposed on a world- wide scale by Wallace and others and applied more specifically to North America by Merriam (Life-zones), Shelford (Biomes), and Dice (Biotic 537 Provinces). Space does not permit the reproduction of the lengthy papers dealing with these subjects. Four selections in this section (Kurtén, Guilday, Koopman and Martin, and Findley and Anderson) deal with various zoogeographic problems related to Pleistocene, subfossil, and Recent faunas, whereas another (Brown) ex- amines the nonequilibrium insular nature of mammals isolated on mountain tops. The short paper by Hansen and Bear contrasts pocket gophers from different environments in Colorado. D. E. Wilson’s contribution compares bat faunas from six different zoogeographic regions using trophic groupings. Those of Hagmeier and J. W. Wilson III, are attempts from different points of view to analyze distributional patterns of North American mammals, both based on initial compilations from one of the faunal catalogues (Hall and Kelson) cited above. 538 Eiszeitalter und Gegenwart Band 14 Seite 96-103 [Obringen!Wire, 1. September 1963 Notes on some Pleistocene mammal migrations from the Palaearctic to the Nearctic Von ByOrn Kurten, Helsingfors Mit 2 Abbildungen im Text Summary. The following dates for mammalian migrations from the Palaearctic to the Nearctic are sueee ne Smilodontine sabre- tooths, Elster (Kansan); black bears, Elster (Kansan); brown and grizzly bears, Wiirm (Wisconsin); wolverine, Saale (Illinoian). Correlation between the mammalian faunas in the Nearctic and the Palaearctic should be based on compilation of many additional migration items. Zusammenfassung. Die Einwanderungen einiger palaarktischer Saugetiere ins Nearkti- kum werden folgendermaffen datiert: Smilodontine Sabelzahnkatzen Elster (Kansan). Schwarz- biren Elster (Kansan). Braunbaren, bzw. Grizzlybaren Wiirm (Wisconsin). Vielfraf§ Saale (IIli- noian). Fiir eine befriedigende Korrelation zwischen den eiszeitlichen Saugetierfaunen des neark- tischen und palaarktischen Raumes miiften noch eine Reihe von Einwanderungsbeispielen analysiert werden. The correlation between the Pleistocene mammalian faunas of North America and Europe is at present a topic of much informal discussion and controversy, but on which relatively little has been published. The knowledge of Pleistocene faunal evolution in both areas is still incomplete, more so in the Nearctic, but a fairly coherent succession has recently been worked out by Hrssarp and his associates (Hipparp, 1958; Tayvtor & Hipparp, 1959) and related to the standard glacial-interglacial sequence. Perhaps it may still be said that knowledge is too incomplete to permit a stage-by-stage correlation on faunal evidence. Nevertheless the topic is of such interest that contributions to it should be welcomed. It appears to the present writer that the most hopeful method to attack the problem is the detailed study of case histories of intercontinental migration by means of taxonomic and evolutionary analysis. Hence I have chosen to offer some notes on a number of Carnivora, summarized from a comparative study in progress. They are intended to supply some preliminary correlation items of the desired kind. It may per- haps be hoped that specialists on this and other groups would analyse other instances of intercontinental migration in the Pleistocene, of which many would be available. It may be assumed that migration between the Old and the New World occurred exclusively across the Bering Strait, as far as the mammals are concerned, and that it took place only when there was a land bridge; that is to say, during a glacial phase. Immigrants are therefore assumed to have migrated in the preceding cold phase, if their first occurrence is in an interglacial fauna. First occurrence in a cold fauna is taken to signify an immigration during the same cold phase. In either case, however, it is a prere- quisite that a probable ancestor should be known to have existed, at the given time, in the area of assumed origin. Errors are bound to arise sometimes because our knowledge is incomplete and later discoveries may reveal that the immigrant was actually present at an earlier date. A more detailed analysis of the evolving populations may help us to avoid errors of this kind. If it can be shown that the assumed ancestor and the immigrant form an essential mor- phological continuum, this may be taken as additional indication that the correct time of migration has been found. A morphological gap between the two will suggest that part of the evolutionary sequence is missing and may have taken place in either area. I have endeavoured to pay full attention to this factor in the examples to follow. 539 Pleistocene mammal magrations from the Palaearctic to the Nearctic 97 A. Sabre-tooths of the genera Megantereon and Smilodon The close relationship between the European Megantereon and the American Smilodon was recognized by Scuaus (1925). Unfortunately, however, Matruew (1929) made the error of synonymizing the European Homotherium with Smilodon. With the discovery of excellent material of the sabre-tooth Dinobastis in the late Pleistocene of Texas (Meape, 1961) it has become clear that this form, not Smilodon, is the American ally of the European Homotherium, whereas Megantereon is allied to Smilodon. They form two quite distinct groups of sabre-tocthed cats, which may be termed the tribes Homotheriini and Smilodontini. ScHauB (1925) pointed to the detailed similarity in the postcranial skeletons of Megantereon and Smilodon. The neck, for instance, is much elongated, and the distal segments of the heavy limbs are shortened. In the Homotheriini the neck is less elongated and the limbs are not shortened distally, indeed the forearm is extremely long. The dentitions and skulls (fig. 1) are also quite distinctly constructed in the two groups. The Smilodontini have dirk-like, very long upper canines, which were evidently used for stabbing exclusively; they are relatively and absolutely larger in Smilodon, but this is only a specialized character and does not obscure the essential similarity. The lower canines were reduced and form flanking elements in the transverse incisor row. The cheek teeth are not much modified from the normal feline type, except for a progressive reduction of the anterior elements and of the protocone (internal cusp) in the upper carnassial. The skull profile tends to be triangular, with a high occiput, only slightly overhanging the occipital condyles. The post-orbital processes are well set off with a marked con- striction behind, separating them from the small but globular braincase. The development of the mastoid prcecesses is correlated with that of the head depressors and is more pronounced in the advanced Smilodon with its enormous sabres. In contrast, the Homotheriini have relatively short, flattened sabres with crenulated, sharp cutting edges all along the front and back; wear facets show that they were used in biting, as well as stabbing and slashing. The incisors form a semicircle, unlike the Fig. 1. Skulls of Homotheriini (left) and Smilodontini (right) in side view. Upper left, Homotherium crenatidens, Perrier, Villafranchian. Lower left, Dinobastis serus, Friesenhahn (Texas), Wisconsin. Upper right, Smilodon neogaeus, Arroyo Pergamino (Argentina), Pampean. Lower right, Megan- tereon megantereon, Senéze, Villafranchian. Not to scale. 7 Eiszeit und Gegenwart 540 98 Bjorn Kurtén smilodont transverse row. The cheek teeth are highly modified, extremely thin slicing blades. The skull is long and low with an arched profile, the frontal region is broad without distinctly set off processes, and the braincase is separated from the occipital plane by a marked constriction. The two tribes probably arose independently from orthodox feline cats by divergent evolution along quite different adaptive paths. The first stage in the development of sabre-like upper canines is seen in the present-day Felis nebulosa. The idea of an iterated evolution of sabre-toothed cats gains in credibility from the fact that independent evolu- tion of sabre-toothed carnivores has been demonstrated in the Marsupialia and Creodonta. The history of both groups is mainly or entirely contained in the Pleistocene (inclu- ding the Villafranchian), and most or all of the Eurasian and American Pleistocene sabre-tooths may be referred to one group or the other. The two main types of homotheres, Homotherium and Dinobastis, occur in both hemispheres. The former are only early Pleistocene (Villafranchian) in Europe, but may occur later in America (Ischyrosmilus?). The latter are middle and late Pleistocene (Dinobastis serus, North America; Dinobastis latidens, Europe; Dinobastis ultimus, China). The smilodont cats show a more definite evolutionary trend and indicate an inter- continental migration at a rather narrowly defined point in time. All the Eurasian forms are referred to the genus Megantereon. The earliest forms, apart from some possible Indian ancestors in the Pliocene, occur in the earliest Villa- franchian in Europe (Villafranca d’Asti, Etouaires). They are relatively small, of perhaps puma size. There is evidence of a gradual size increase, and the late Villafranchian forms (Senéze, Val d’Arno, Nihowan) are somewhat larger. All of the European Villafranchian (\ Lee, Fig. 2. Evolution of lower jaw and teeth in the Smilodontini. Bottom, Megantereon megantereon, Senéze, Villafranchian, with Ps and large jaw flange. Centre, Smilodon gracilis, Port Kennedy Cave, Yarmouth, retaining P3 (alveolus), flange somewhat reduced. Top, Smuilodon neogaeus, Lapa Escrivania, Brazil, late Pampean, size greatly increased, Ps lost, flange reduced. All to the same scale. 541 Pleistocene mammal magrations from the Palaearctic to the Nearctic 99 populations may, however, be referred to a single evolving species, M. megantereon. At the close of the Villafranchian, the line became extinct in Europe, but in Asia (and Africa) it survived into the middle Pleistocene. The last representative of this line in Asia, known at present, is Megantereon inexpectatus from Locality 1 (the Peking Man site) of Chou- koutien. The date of this form is late Elster or early Hoxnian. M. inexpectatus is larger than M. megantereon, showing that the phyletic growth continued, and in fact it is about the same size as the earliest American Smilodons, Our next glimpse of this evolutionary line comes from the New World with the ear- liest known members of the genus Smilodon. They come from Port Kennedy Cave out of deposits that appear to be Yarmouth in age (Hipparp, 1958). As fig. 2 shows, these forms resemble advanced Megantereon more than advanced Smilodon in many characters. They still retain a well developed P3 (alveolus in the figured specimen) and have a distinct inner cusp (protocone) in the upper carnassial. On the other hand, the reduction of the dependent flange on the lower jaw has already got under way in the early Smilodon. The trend in this character, within Smilodon, shows well enough that the genus evolved from a large-flanged ancestor like Megantereon. Apparently the sabre still bit inside the lower lip in Megantereon, and had to have a sheath supported by the jawbone. In Smilodon the sabre bit outside of the lower lip, and the sheath could be reduced. If this character is made the key character of the two genera, the Port Kennedy Cave form should go into Smilodon in spite of numerous resemblances to Megantereon. The development of the jaw flange in the Choukoutien form is unfortunately unknown (TErLHarD, 1945). In Smilodon of Illinoian age, from the Conard Fissure (Brown, 1908), further pro- gress in size and dental characters have occurred, but not until Sangamon and Wisconsin time the full-fledged Smilodon known from Rancho La Brea and other asphalt deposits is met with. It appears highly probable that the migration occurred at a point in time roughly coinciding with the age of the Jast known Megantereon. Thus the migration would be likely to be of Elster date. In this way it may be concluded that the characteristic Elster faunas of the Old World antedate the Yarmouth faunas in North America, and that the Yarmouth is a correlative of the European Holstein. Smilodon also entered South America, where the earliest form, a relatively small and primitive one, occurs in the Chapadmalal (Krac.ievicn, 1948). This appears to give a maximum age for the Chapadmalal: it can hardly antedate the Yarmouth and Holstein. The outlines of the evolution and migration of the Smilodontini are indicated in the diagram (table 1). B. Bears of the genus Ursus The bear family, Ursidae, is one of the smallest and most recent carnivore families. Three subfamilies are recognised at present (THENtus, 1958, 1959), but one, the Agrio- theriinae, became extinct at the close of the Pliocene, and does not concern us here. An- other, the Tremarctinae, is exclusively American in distribution, and evolved from immi- grants dating back to the Pliocene (Plionarctos). The presence of large tremarctine bears (Arctodus) may have been a factor in the relatively late spread of Ursus into the New World. The third subfamily, the Ursinae, has a Holarctic and Indian distribution. With a single exception (Ursus americanus) all of its species are present in the Old World, and the fossil record shows that it originated in Eurasia. In the Nearctic, ursine bears are not known until the middle Pleistocene, with a single uncertain exception (JoHNsTON & SavAGE, 1955), a specimen from the Blancan Cita Canyon; it is fragmentary and may, or may not, be ursine. 542 100 Bjorn Kurtén Table 1 Evolution and migration of the Smilodontini South America North America Eurasia Slog Smilodon ae a Wisconsin | “californicus* Wiirm ERE CHS (Rancho La Brea etc.) Sangamon spied Eem Smilodon : ensenadensis F lod — Illinoian Sk retaide Rif-Saale S. riggii Conard Fissure Chapadmalal * S. gracilis : eel. soe Yarmouth Boe Kennedy Cave ae ‘ Megantereon aaa aa ge oa a oe inexpectatus se Choukoutien Cromer Megantereon spp. & Villa- See es M. megantereon Table 2 Intercontinental migrations of Ursus, excluding U. maritimus North America Eurasia a ees Recent U. americanus U. arctos Recent U. arctos U. thibetanus U. americanus U. arctos<- | — — — — | U.arctos U. thibetanus Wisconsin Many locs. Alaska Many locs. China Wirm Gee on U. americanus Fen U. arctos U. thibetanus rae ei Trinity River Many locs. China U. americanus U. arctos U. thibetanus Illinoian Cumberland Cave, Conard Rif-Saale | Tornewton Cave Europe, China Fissure etc. U. americanus ? U. arctos U. thibetanus Yarmouth Port Kennedy Cave ADB Grays etc. China f | Mindel- U. arctos Elster China | U. thibetanus es China Gronies U. thibetanus China, Europe Villa- U. etruscus U. ethibetanus franchian Europe China 543 Pleistocene mammal magrations from the Palaearctic to the Nearctic 101 The first certain ursine species to appear in North America is Ursus americanus, the black bear. The earliest record appears to be Port Kennedy Cave, as in the case of the smilodonts, and the bears evidently date from the Yarmouth. These early black bears are of moderate size and have several primitive characters, e.g. the large size of the upper carnassial and the small size of the last molar. In these characters, and also in morphology, the Port Kennedy Cave black bear closely resembles the middle Pleistocene Ursus thibe- tanus kokeni (Asiatic black bear) known from Chinese deposits, e. g. Choukoutien. It seems probable that the American form descended directly from the closely allied Asiatic species, and that the migration occurred at the same time as that of the Smilodontini, i. e. during the Elster Glaciation. Illinoian black bears in North America, from Cumberland Cave and Conard Fissure (Giptey & Gazin, 1938), show definite advance over the stage seen at Port Kennedy. Late Pleistocene forms reached great size; in the Postglacial, the size was secondarily reduced (KurrTEn, in the press). Two other species of Ursus are at present found in North America, the polar bears (Ursus maritimus) and the brown and grizzly bears (Ursus arctos). Both are conspecific with Old World species, and the indication is that their migration is of more recent date. Unfortunately the fossil history of the polar bear is practically unknown. As regards Ursus arctos, however, the fossil record bears out the contention. Most or all fossils of this species from North America appear to date from Postglacial times or possibly the latest Wisconsin (KuRTEN, 1960). It is possible that the species was present in Alaska at a somewhat earlier date, well back in the Wisconsin. However this may be, the intercon- tinental migration evidently took place during the Wiirm = Wisconsin. As a matter of fact, the morphology of the Alaskan and Eastern Siberian Ursus arctos indicates two independent migrations: a northern, with narrow-skulled animals from northern Siberia, and a southern, with broad-skulled animals from the Kamchatka population. C. The glutton, Gulo gulo The glutton or wolverine evolved in the Old World. The ancestral form is the Cromerian Gulo schlosseri, known from various localities in Central Europe. and chiefly distinguished by its much smaller size. The first true Gulo gulo appear in the Elster (Mos- bach; see Topren, 1957) of Europe, and also in China (Choukoutien; see Per, 1934), In North America, the earliest record of wolverine appears to come from Cumberland Cave (GiwLey & Gazin, 1938), where it is part of the cold elements that appear to date from the Illinoian (Hrsparp, 1958). The Illinoian is thus the minimum age of the migra- tion, but there is also a possibility that the migration dates back to the Elster. It may be noted, however, that the New World population is only very moderately differentiated from that in the Old (Kurtin & Rauscu, 1959), and only ranks as a distinct subspecies. This would support a relatively late date, and at present a Saale-Illinoian migration appears the most likely alternative. Conclusions The three migration items discussed here support the correlation of glaciations and interglacials in North America and Europe as far back as the Holstein in Europe and Yarmouth in North America, as shown in tables 1 and 2. The exact European corre- latives of the Kansan, the Aftonian, and the Nebraskan faunas remain doubtful. Perhaps the definitive clearing up of the migration of the elephants will settle part of the problem. The earliest true elephants in North America appear in faunas assigned to the Kansan, such as the Holloman and Cudahv (Taytor & Hissarp, 1959). This early form is Elephas haroldcooki. Detailed analysis of a large material will be necessary to show whether 544 102 Bjorn Kurtén this species may be derived from the primitive mammoths of the Elster, or from advanced Elephas meridionalis types of the late Villafranchian. A correlation of the Kansan with the Elster would make the Aftonian a correlative of the Cromerian in Europe. The latter is a complex stage with two distinct temperate oscillations (West, 1961). On the other hand, many American specialists seem to favour a correlation of the Aftonian with the Villafranchian in Europe. Some implications of such a correlation are somewhat disturbing. Correlation of the Aftonian or part of it with the Villafranchian, and of the Yarmouth or part of it with the Holstein, would suggest one of the schemes (1)—(3) below, in contrast with the usual arrangement (4). (1) (3) Holstein Yarmouth Holstein Yarmouth (Elster) Kansan Elster Cromer Cromer Kansan Giinz Aftonian (Giinz) Aftonian Villafranchian Villafranchian Nebraskan Donau Nebraskan Donau Rexroadian Astian Rexroadian Astian (2) Yarmouth Holstein (4) Elster Yarmouth Holstein Kansan (Cromer) Kansan Elster Giinz Aftonian Cromer Aftonian Villafranchian Nebraskan Giinz Nebraskan Donau Rexroadian Villafranchian Rexroadian Astian It would obviously be premature to attempt an evaluation of these and other possible combinations at present, when even the intra-continental correlations (e. g., the dating of the American faunal sequence in terms of the American glacial-interglacial sequence) are somewhat uncertain. One possible source of bias in intercontinental correlation should, however, be mentioned. Strictly homotaxial relations for migrating groups can only be expected at the time of the actual migration, i.e., at the time of a glaciation, as a rule. Apparent homotaxial relations between interglacial faunas may be deceptive. For a hypo- thetical example, suppose that a typical Holsteinian Old World form migrates to North America in the Saale (Illinoian), and becomes extinct in Eurasia, or perhaps evolves into a more advanced Eemian type. If it is further supposed that the American immigrant happens to be known to us only in strata of Sangamon age, this will be a case of closer homotaxial relationships between the Sangamon and the Holstein, than between the Sangamon and the Eem. This may possibly have some bearing on the apparent relation- ship between the Aftonian and the Villafranchian, Naturally, migrants in the other direction, from the New World to the Old, will have the opposite effect; but as these migrations have been much less common, their effect is likely to be overshadowed. Numerous migration items await detailed analysis. Lynxes among felids; wolf and red fox among canids; least weasel, otter and marten among mustelids are obvious cases in the Carnivora, and the only known American hyaenid may be added: Chasmaporthetes, which appears in the early Pleistocene Cita Canyon fauna and has a close relationship with the European Euryboas, the ,sprinter hyena“. The importance of the Proboscidea has already been stressed, and numerous examples will be found among the rodents. Horses and camels exemplify migration from the New World to the Old, perhaps a subsequent remigration of modernized Equus into North America (McGrew, 1944). Elk 545 Pleistocene mammal migrations from the Palaearctic to the Nearctic 103 (Alces), reindeer (Rangifer), yak (Bos), bison (Bison), musk ox (Ovibos) and sheep (Ovis) are important artiodactyl migrants from the Old World to the New, most of them in the late or latest Pleistocene. References Brown, Barnum: The Conard Fissure, a Pleistocene bone deposit in northern Arkansas: With description of two new genera and twenty new species of mammals. - Mem. American Mus. Nat. Hist. 9 (4), 157-208, New York 1908. Giwiey, J. W., & Gazin, C. L.: The Pleistocene vertebrate fauna from Cumberland Cave, Mary- land. - Bull. U.S. Nat. Mus. 171, 1-99, Washington 1938. Hrpparb, Claude W.: Summary of North American Pleistocene mammalian local faunas. - Papers Michigan Acad. Sci. 43, 3-32, Ann Arbor 1958. Jounston, C. S., & Savace, D. E.: A survey of various late Cenozoic vertebrate faunas of the Panhandle of Texas, part I: Introduction, description of localities, preliminary faunai lists. - Univ. California Pub!. Geol. Sci. 31, 27-50, Berkeley 1955. KRAGLIEVICH,Lucas Jorge: Smilodontidion riggii, n. gen. n. sp. Un nuevo y pequefio esmilodonte en la fauna pliocena de Chapadmalal. - Rev. Mus. Argentino Ci. Nat. 1, 1-44, Buenos Aires 1948. KurtEn, Bjérn: A skull of the grizzly bear (Ursus arctos L.) from Pit 10, Rancho La Brea. - Los Angeles County Mus. Contr. Sci. 39, 1-7, Los Angeles 1960. KurteEn, Bj6rn & Rauscu, Robert: Biometric comparisons between North American and European mammals. - Acta Arctica 11, 1-44, Copenhagen 1959. McGrew, Paul O.: An early Pleistocene (Blancan) fauna from Nebraska. - Geol. Ser. Field Mus. Nat. Hist. 9, 33-66, Chicago 1944. Mattuew, William D.: Critical observations upon Siwalik mammal!s. - Bull. American Mus. Nat. Hist. 56 (7), 437-500, New York 1929. MEapE, Grayson E.: The saber-toothed cat Dinobastis serus. - Bull. Texas Memor. Mus. 2, 25-60, Austin 1961. Pet, Wen-chung: On the Carnivora from Locality 1 of Choukoutien. - Palaeont. Sinica, ser. C, 8, 1-216, Peking 1934. Scuaus, Samuel: Uber die Osteologie von Machaerodus cultridens Cuvier. - Ec!og. geol. Helv. 19, 255-266, Basel 1925. Taytor, Dwight D. & Hrsparn, Claude W.: Summary of Cenozoic geo!ogy and paleontology of Meade County area, southwestern Kansas and northwestern Oklahoma. - Pamphlet, 1-157, Ann Arbor 1959. TEILHARD DE Cuanpin, Pierre: Les formes fossiles. - Les félidés de Chine, 5-35, Peking 1945. THENIUuS, Frich: Uber einen Kleinbiren aus dem Pleistozin von Slovenien nebst Bemerkungen zur Phylogenese der plio-pleistozinen Kleinbaren. - Razprave Slov. Akad. Znan. 4, 633-646, Ljubljana 1958. - - Ursidenphy'ogenese und Biostratigraphie. - Zeitschr. Sauge- tierk. 24, 78-84, Berlin 1959. Tosren, Heinz: Cuon Hope. und Gulo Friscu (Carnivora, Mammalia) aus den altpleistozanen Sanden von Mosbach bei Wiesbaden. - Acta Zool. Cracoviensia 2, 433-452, Krakéw 1958. West, R. G.: The glacial and interglacial deposits of Norfo'k. - Trans. Norfolk & Norwich Nat. Soc. 19, 365-375, Norwich 1961. Manuskr. eingeg. 3. 1. 1963. Anschrift des Verf.: Dr. B. KurtéN, Zoologisches Museum der Universitat, N. Jarnvagsgatan 13, Helsingfors, Finnland. 546 PLEISTOCENE ZOOGEOGRAPHY OF THE LEMMING, DICROSTONYX} Joun E. GuILpAy Carnegie Museum, Pittsburgh, Pa. Received August 30, 1962 The collared lemmings, genus Dicros- tonyx Gloger, are currently divided into two subgenera. Misothermus Hensel con- tains a single species, D. hudsonius Pallas, isolated on the tundra of northern and coastal Ungava from all other Dicrostonyx (see fig. 1). The subgenus Dicrostonyx Gloger contains the remaining species of the genus, D. torquatus Pallas of the palae- arctic, D. groenlandicus (Traill) of the nearctic, and D. exsul G. M. Allen confined to St. Lawrence Island in the Bering Straits. The torquatus-groenlandicus-exsul species group may be conspecific as inti- mated by Ellerman and Morrison-Scott (1951, p. 653). It is clear that they are more closely related to one another than to the isolated D. hudsonius. In the absence of any fossil record and interpreting on the basis of modern geo- graphical distribution alone, one might argue that the differentiation of D. Audson- tus dated from the Wisconsin glaciation; that as the ice front and its presumed periglacial tundra belt shrank to the north, the eastern segment of the retreating lem- ming population was cut off by Hudson Bay. The bay eventually cut the Canadian tundra into an eastern and a western com- ponent, each with its distinctive form of collared lemming. This does not appear to be the case, however. The inaccuracy of this interpretation is shown by the fossil record. The one record from the North American Pleistocene, frag- mentary skulls and mandibles of at least four individuals from Sinkhole no. 4, New Paris, Pennsylvania (Guilday and Doutt, 1961), is that of typical Misothermus (for characters, see Miller, 1898; Hinton, 1926; 1 Research conducted under National Science Foundation Grant no. G-20868. Evotution 17: 194-197. June, 1963 Hall and Kelson, 1959), indistinguishable from the modern D. hudsonius. Carbon particles taken from a position five feet higher in the sinkhole matrix were dated at 11,300 + 1,000 years (Yale Univ. lab. no. 727). The age of the lemming remains is somewhat in excess of this. The Mizso- thermus dental pattern was fixed prior to the Wisconsin recession and the formation of present Hudson Bay. There have been two species of collared lemmings described from the palaearctic Pleistocene. Dicrostonyx gulielmi Sandford based upon cranial material from Hutton Cave, Somersetshire, England, is a late Pleistocene form of the living D. torquatus, and may be conspecific with it (see Kowal- ski, 1959, p. 229). It is a common Eur- asian Pleistocene fossil. The second Old World fossil form, D. henseii Hinton, described from cranial material from a fissure deposit at Ightham, Kent, England, appears to be a typical Misothermus (see the description by Hin- ton, 1926, p. 163). D. (Misothermus) henseli has been recorded from the Pleis- tocene of England, Ireland, Jersey, France, and Germany (Hinton, 1926; Brunner, various papers); D. (Dicrostonyx) tor- quatus (or gulielmi), from the Pleistocene of England, Ireland, France, Poland, Czech- oslovakia (Hinton, 1926; Kowalski, 1959; Fejfar, 1961). This by no means exhausts the list of Old World Pleistocene Dicro- stonyx localities. But enough has been cited to indicate a geographical and pos- sibly a chronological overlap between the two species. Both forms were recovered by Hinton from Merlin’s Cave, Wye Valley, Herefordshire, England (22 D. gulielmi skulls, 4 D. henseli) and at Langwith Cave, Derbeyshire (1 D. gulielmi, 2 or 3 D. hen- seli). Brunner recorded D. henseli from 194 547 ZOOGEOGRAPHY OF DICROSTONYX 195 Fic. 1. A. Mainland modern distribution of the subgenus Dicrostonyx in America. B. Modern distribution of the subgenus Misothermus. thirteen Bavarian cave deposits. In one, the Markgrabenhohle, Brunner (1952c, p. 465) reported that 25% of the mandibles resembled D. gulielmi in possessing a small anteroexternal vestigial angle on Ms, ‘‘eine deutliche aiissere Schmeltzfalte.” Many uncorrelated fissure, cave, and terrace de- posits are involved, however. And while they are all middle to late Pleistocene in age, their sequential position within that time span has not been established with any degree of confidence. Outline map of North America, showing approximate limit of continental glaciation. The facts at hand seem to indicate that two forms of the genus Dicrostonyx inhab- ited Eurasia and perhaps North America during the Pleistocene, and that one of them survives as a postglacial relict, isolated in the tundra of Ungava (fig. 2). The pre- Wisconsin origin of the Misothermus dental pattern is demonstrated by fossil forms in both continents. If we assume, as does Hinton (1926), that Misothermus is not a true phylogenetic category but that D. henseli and D. hud- 548 196 JOHN E. GUILDAY Fic. 2. sonius are of independent origin from Dicrostonyx proper, we are faced with the apparent coincidence that a form (henseli) was replaced by modern Dicrostonyx in the Old World while its morphological equiva- lent, D. hudsonius, which ranged as far south as central Pennsylvania during late Wisconsin times, survives today only where it is completely isolated from all contact with the Eurasian-Western Nearctic Dicro- Stonyx. Both D. henseli and D. hudsonius appear Postulated distribution of Dicrostonyx (A) and Misothermus (B) in North America at Wisconsin glacial maximum. Note site of Sinkhole no. 4, New Paris, Bedford County, Pennsylvania. Hachures indicate approximate limit of continental glaciation. to have been completely or partially re- placed by true Dicrostonyx. Is it possible that modern D. hudsonius (or some form of Misothermus) at one time ranged through- out the holarctic, and that it was replaced during late Pleistocene times by lemmings of the subgenus Dicrostonyx, first in the Old World, later in the New; this latter replacement occurring sometime after the post-Wisconsin formation of Hudson Bay and the division of the mainland North 549 ZOOGEOGRAPHY OF DICROSTONYX American tundra into an eastern and a western component? I wish to thank Dr. J. Kenneth Doutt, Curator of Mammals, Miss Caroline A. Heppenstall, Assistant Curator of Mam- mals, and Dr. Craig C. Black, Gulf Associ- ate Curator of Vertebrate Fossils, Carnegie Museum, for their helpful criticism. SUMMARY The modern distribution of Dicrostonyx hudsonius Pallas (confined to the tundra of Ungava) is believed, on the basis of the fossil record, to be a relict of a former holarctic pre-Wisconsin distribution. REFERENCES CITED BRUNNER, GEORG. 1949. Das Gaisloch bei Miin- zinghof (Mfr.) mit Faunen aus dem Altdiluvium und aus jiingeren Epochen. Neuen Jahrbuch Mineral., etc. Abhandlungen, 91(B): 1-34. 1951. Eine Faunenfolge von Wirm III Glazial bis in das Spat-Postglazial aus der “Quellkammer” bei Pottenstein (Ofr.). Geol. Bl. NO-Bayern, 1: 14-28. 1952a. Das Dohlenloch bei Pottenstein (Obfr.). Eine Fundstelle aus dem Wirm II Glazial. Abhandlungen Naturhist. Ges. Nurn- berg, 27(3): 49-60. 1952b. Der “Distlerkeller” in Pottenstein Ofr. Eine Faunenfolge des Wiirm I-III inter- stadial. Geol. Bl. NO-Bayern, 2: 95-105. 1952c. Die Markgrabenhohle bei Potten- stein (Oberfranken). Eine Fauna des Altdi- luviums mit Talpa episcopalis Kormos u.a. Neues Jahrbuch Geol. Palaontol. Mh., 10: 457-471. 1953a. Die Heinrichgrotte bei Burggaillen- reuth (Oberfranken). Eine Faunenfolge von Wiirm I-Glazial bis Interstadial. Neues Jahr- buch Geol. Palaontol. Mh., 6: 251-275. 1953b. Die Abri “Wasserstein” bei Betzen- stein (Ofr.). Eine subfossile Fauna mit Sorex 197 minutissimus H. de Balsac. Geol. Bl. NO- Bayern, 3: 94-105. —. 1955. Die Hohle am Butzmannsacker bei Auerbach (Opf.). Geol. Bl. NO-Bayern, 5: 109-120. —. 1956. Nachtrag zur Kleinen Teufelshohle bei Pottenstein (Oberfranken). Eine Ubergang von der letzten Riss-Wirm-Warm-fauna zur Wiirm I-Kaltfauna. Neues Jb. Geol. Palaontol. Mh., 2: 75-100. 1957a. Die Breitenberghohle bei Gdsswein- stein/Ofr. Eine Mindel-Riss-und eine post- glaziale Mediterran-Fauna. Neues Jb. Geol. Palaontol. Mb., 7-9: 352-378, 385-403. 1957b. Die C§aciliengrotte bei Hirschbach (Opf.) und ihre fossile Fauna. Geol. Bl. NO- Bayern, 7: 155-166. 1958. Das Guckerloch bei Michelfeld (Opf.). Geol. Bl. NO-Bayern, 8: 158-172. 1959. Das Schmeidberg-Abri bei Hirsch- bach (Oberpfalz). Palaont. Z., 33: 152-165. ELLERMAN, J. R., AnD T. C. S. Morrison-Scort. 1951. Checklist of Palaeoarctic and Indian mammals. British Museum (Natural History). London. 810 p. FEJFAR, OLDRICH. 1961. Review of Quaternary Vertebrata in Czechoslovakia. Instytut Geo- logiczny. Odbitka z Tomu 34 Prac. Czwar- torzed Europy Srodkowej I Wschodniej, p. 109-118. Guitpay, J. E., AnD J. K. Doutr. 1961. The Col- lared Lemming (Dicrostonyx) from the Penn- sylvania Pleistocene. Proc. Biol. Soc. Wash- ington, 74: 249-250. Hatt, E. R., AnD R. K. Ketson. 1959. The mam- mals of North America. Vol. II, p. 547-1083. Hinton, M. A. C. 1926. Monograph of the voles and lemmings (Microtinae) living and ex- tinct. Vol. I. Richard Clay and Sons, Suffolk. 488 p. KowatskI, K. 1959. Katalog Ssakow Plejstocenu Polski. Polska Akademia Nauk. Inst. Zool. Oddzial W Krakowie. 267 p. Miter, G. S., JR. 1896. Genera and subgenera of voles and lemmings. North American Fauna no. 12, 80 p., U. S. Dept. Agriculture. 550 SUBFOSSIL MAMMALS FROM THE GOMEZ FARIAS REGION AND THE TROPICAL GRADIENT OF EASTERN MEXICO By Karz F. KooOpMAN AND Paut S. MARTIN In the spring of 1953 Byron E. Harrell and P. S. Martin collected superficial animal remains at three cave localities in the Sierra Madre Oriental of south- western Tamaulipas. Locally, the mountains are sufficiently humid to support small, isolated patches of Cloud Forest and Tropical Evergreen Forest ( Martin, 1958). At this latitude, 23° north, these two tropical plant formations appear to reach their limit. In recent years four faunal papers on mammals of southern Tamaulipas have appeared, each reporting certain tropical species unknown at higher latitudes (Baker, 1951; Goodwin, 1954; Hooper, 1953; de la Torre, 1954). Southern Tamaulipas appears to be of primary significance in the Gulf lowlands faunal gradient, a system extending from southern Veracruz _ to southern Texas. In the lowlands of eastern Mexico many of the dominant tropical American taxa reach their range limits. We seek to define the north- eastern section of this gradient with regard to tropical mammal faunas, to relate it to shifts in vegetation and to indicate the relative importance of the Gomez Farias region as a faunal terminus. The Gomez Farias region is defined as the area from 22°48’ to 23°30’ north latitude and 99° to 99°30’ west longitude, or approximately the rectangle enclosed by the towns of Llera, Jaumave, Ocampo and Limon. In establishing the presence of eight species known in the Gomez Farias region only from the skeletal remains, and in extending the altitudinal or ecological ranges of others, the present collection supplements previous reports. It indicates the value of using owl pellet deposits as a cross check on standard trapping technique. DESCRIPTION OF DEPOSITS Cretaceous limestones comprising the precipitous east slope of the Sierra Madre Oriental near the village of Gomez Farias are severely folded. Under torrential summer rains they have eroded into very rough karst terrain with virtually no surface drainage. Caves and sink holes, a characteristic of karst, are a common feature. Most do not appear to be inhabited by bats or owls. Of those that are, the constant high humidity and frequent flushing from 1 551 9 JOURNAL OF MAMMALOGY Vol. 40, No. 1 percolating rainwater apparently prevent accumulation of deep bone or guano deposits. Large bat colonies numbering thousands of individuals occur in Tropical Deciduous Forest in the Canyon of the Rio Boquilla, 8 km. southwest of Chamal, and in a guano cavern at El Abra, 8 km. northeast of Antiguo Morelos. However, no colonies of similar size have been found in the more humid portions of the Gomez Farias region. Of approximately thirty caves and sink holes explored near Gémez Farias, material from three is represented in our collection. All occur in the mountains west of the village of Gémez Farias, latitude 29°03’ north, longitude 99°09’ west, and within 16 km. of each other (see Table 1). The following information will serve to characterize them: 1. Paraiso. Aserradero del Paraiso is the name of a small sawmill located in Tropical Evergreen Forest 13 km. north-northwest of Chamal. A narrow ravine about 1 km. south of the sawmill harbors several caves, including a deep, wet grotto with permanent water. On the sloping floor of a small TaBLE 1.—Mammals from cave deposits in the Gémez Farias region (numbers refer to anterior skull parts identified) PARAISO RANCHO DEL CIELO INFERNO Distance from Gémez Farias: 13 km. SW 6 kn. NW 7 km. W Elevation in meters: 420 1050 1320 Vegetation type: Tropical Ever- Cloud Forest Cloud Forest green Forest Didelphis marsupialis ________.- san — — 1 Marmosa mexicana ————______ —_ — 18 Cryptotis pergracilis _.._____ 3 Cryptotis mexicana _____.___-_____-_- —_ 1 10 Chilonycteris parnellii _._____— I Enchisthenes harti —.._______~ -— -— tr Artibeus cinereus —.__..___ _— 3 Centurio senex _.______- noes — _ 1 Eptesicus fuscus ————___.._— 1 Lasiurus cinereus __..____- aes — — 1 Antrozous pallidus —.___ 1 Sylvilagus floridanus ______ 1 Glaucomys volans _______-___ i 1 12 Liomys irroratus —___...._________ 1 Reithrodontomys mexicanus ____— _ 2 5 Reithrodontomys megalotis —_____ — —_ 1 Baiomys taylori ___.-__-___.. ee 1 Peromyscus boylet ——_.__-.__- a 1 17 Peromyscus pectoralis ___._____ —_ — 2 Peromyscus ochraventer —____ — — 7 Oryzomys alfaroit 3 — 5 Sigmodon hispidus _..___. eae ae 29 Neotoma angustapalata _._______. 9 1 17 Total identifications __...____ 51 9 98 552 Feb., 1959 KOOPMAN AND MARTIN—MAMMALS OF EASTERN MEXICO 3 dry cave on the west wall of this ravine many scattered (apparently water- transported) small bones were found. 2. Rancho del Cielo. A small sink and cave several hundred meters east of this important Cloud Forest collecting locality contained a few bat remains and fresh owl pellets. 3. Inferno (also designated Infernillo). A rather large cave adjacent to an abandoned sawmill of this name is located in upper Cloud Forest roughly 2 km. south of the mill settlement called La Gloria. Abundant pellet remains were found on a dislodged boulder just inside the cave mouth. All the caves are surrounded by heavy forest, much of it recently lumbered. Jagged, shrub-covered or almost bare karst ridges and pinnacles confine the areas of tall forest to valleys, pockets and gentle slopes. A more complete description of the Gémez Farias region is in preparation (Martin, 1958). Although the barn owl, Tyto alba, occurs in a very large cavern at El] Abra north of Antiguo Morelos, the only raptor definitely known to roost in caves in the Gémez Farias region is the wood owl, Ciccaba virgata. While it is possible that certain non-volant mammals died from other causes, all skeletal remains of these, and perhaps even some of the bats, can be ascribed to Ciccaba. Cave records do not make ideal locality data, especially when information on ecological or altitudinal distribution is sought. We assume that the forest types and the elevation in the immediate vicinity of each cave represent the habitat in which the owls fed, but this is by no means certain. The hunting range and nocturnal movements of Ciccaba are unknown. There is no stratigraphic evidence for assuming that any material is older than very recent. Limestone deposit on certain bones may represent the concretion of a single rainy season. SYSTEMATIC TREATMENT OF THE MAMMALS We emphasize first that only a fraction of the mammalian and none of the bird bones have been identified. Very little attempt has been made to identify any of the post-cranial elements, and in the case of the cricetine rodents only the best of cranial material could be identified with any confidence. Particular difficulty was encountered with lower jaws of cricetines, even when teeth were present. As a result, determinations in this group are considered less reliable than in the others. In particular this applies to the Peromyscus— Baiomys-Reithrodontomys group of genera, in which not only specific but also good generic characteristics were hard to find in most of the material. Size, molar form, palatal morphology and shape of the zygomatic plate were found to provide the most useful taxonomic characters in this subfamily. In many cases a closely adhering limestone drip deposit was present and was sometimes difficult to remove without damaging the underlying bone. No attempt has been made to identify subspecies. In our opinion the theoretical requirements of population sampling and measurement, as employed in sub- 503 4 JOURNAL OF MAMMALOGY Vol. 40, No. 1 specific identification, are not met in any but perhaps the best fossil material. For the following species determinations Koopman alone is responsible. Didelphis marsupialis——Inferno: one rostral fragment of a young individual. Previously recorded from Gomez Farias (Hooper, 1953). Marmosa mexicana.—inferno: three rostral fragments and 15 mandibles. On the basis of dentition, these are clearly opossums, but of the Middle Amer- ican genera of Didelphidae, all but Marmosa are much too large. Of the four species of this genus occurring north of Panama, all but M. mexicana differ from the subfossil material either in larger size or greater development of a precondylar crest on the outer side of the mandible. The species has not previously been recorded north of Jalapa, Veracruz. Cryptotis pergracilis——Paraiso: one rostrum and two mandibles. Restriction to the family Soricidae and the genus Cryptotis may be made on the basis of dentition. In eastern Mexico north of the Isthmus of Tehuantepec (states of Tamaulipas, San Luis Potosi, Hidalgo, Puebla and Veracruz) the following six species of Cryptotis are known: C. parva, C. pergracilis, C. obscura, C. micrura, C. mexicana and C. nelsoni. All except C. parva and C. pergracilis may be ruled out on the basis of larger size. While clear-cut cranial differences between the latter two species appear to be absent, the eastern race of per- gracilis, C. p. pueblensis, has a somewhat deeper nasal emargination of the rostrum than the southwestern race of parva, C. p. berlandieri. Though slightly broken anteriorly, the subfossil rostrum appears to have a nasal emargination somewhat closer to that of C. pergracilis pueblensis than to that of the two Tamaulipan specimens of C. parva berlandieri recorded by Goodwin (1954). However, no direct comparison of the Paraiso specimens with C. pergracilis pueblensis was made, but only with a sketch. Unfortunately our material seems inadequate to solve the problem of specific status, i.c., are C. parva and C. pergracilis sympatric in southern Tamaulipas, do they integrade through a narrow hybrid zone, or is there a more complex arrangement? The northernmost previous record of C. pergracilis is Platanito in San Luis Potosi. Cryptotis mexicana.—Inferno: six rostra, four mandibles, and three humeri; Rancho del Cielo: one rostrum. Specimens were trapped at the latter locality (Goodwin, 1954). Chilonycteris parnellii—Paraiso: one mandible. Goodwin (1954) records a series from El] Pachon. As Koopman (1955) has pointed out, the mainland C. rubiginosa and the West Indian C. parnellii are almost certainly conspecific. Since Koopman believed that C. parnellii Gray had several months priority over C. rubiginosa Wagner, the combined species was called C. parnellii. De la Torre (1955) has shown that this is not the case and, finding no way of determining which name was published first, recommended: “In the absence of conclusive evidence, the better known and more widely used name rubiginosa should be retained.” Unfortunately, if there is no clear priority, the law of the first reviser would 504 Feb., 1959 KOOPMAN AND MARTIN—MAMMALS OF EASTERN MEXICO 5 seem to hold, in this case the first to use one of the two names to include both forms, i.e., Koopman (1955). It is not legally possible to withdraw from this position. Therefore it appears that C. parnellii must stand as the name assigned to both mainland and West Indian large Chilonycteris. The question of nomenclature should not obscure the more significant taxo- nomic conclusion that a single species is involved. Artibeus cinereus.—Rancho del Cielo: two partial skulls, one lower jaw. De la Torre has also recorded this species from Rancho del Cielo. Enchisthenes harti—kInferno: one partial skull. The short broad rostrum and characteristic molar pattern rule out all American bats outside the Steno- derminae. Of the Middle American stenodermines, only Uroderma bilobatum, Vampyrops helleri and Enchisthenes harti agree with the Inferno skull in size and dental formula (i? o! p? m*). Both Uroderma and Vampyrops, however, have rostra considerably longer than that of the subfossil skull. On the other hand, there is close resemblance to skulls of Enchisthenes from Honduras and Ecuador. De la Torre (1955) has recently summarized the known records, specimens from Ciudad Guzman in Jalisco being the closest to Tamaulipas geographically. Four other localities extend the distribution south to Trinidad and Ecuador. Centurio senex.—Inferno: one rostrum. Of all the North and Middle Amer- ican bats, only Centurio senex agrees with the subfossil skull in dental formula (i? c! p? m3) and in the palate being more than twice as wide as it is long. The Inferno rostrum resembles a skull of Centurio senex in all important respects. De la Torre (1954) recorded a single specimen from Pano Ayuctle. Eptesicus fuscus.—Paraiso: one mandible. Several characters of this bone immediately narrow the field considerably. These are mandibular length, tooth size, dental formula (is c: pz m3), molar pattern and height of the coronoid process. This leaves us with only two North and Middle American species, Eptesicus fuscus and Dasypterus intermedius. Of these, Dasypterus may be ruled out on the basis of its more robust mandibular ramus. Comparison of the Paraiso mandible with Eptesicus fuscus reveals no important differences. I have been able to find no other records of this bat in Tamaulipas, the nearest localities being Rio Ramos in Nuevo Leén to the west (Davis, 1944) and Cafiada Grande in San Luis Potosi to the southwest (Dalquest, 1953). Good series from Tamaulipas, if they could be obtained, should show integradation between E. f. fuscus and E. f. miradorensis. Lasiurus cinereus—Inferno: one nearly complete skull. All other species of North and Middle American bats may easily be excluded from consideration on the basis of size, rostral shape and dental formula (i! c! p? m*). It matches L. cinereus closely. Since this bat is migratory, it is impossible to say whether this individual belonged to a resident population or was merely a winter visitor. The nearest previous records are Matamoros in northern Tamaulipas ( Miller, 1897) and El Salto in eastern San Luis Potosi (Dalquest, 1953). Antrozous pallidus.—Paraiso: one partial lower jaw. Mandible and tooth 599 6 JOURNAL OF MAMMALOGY Vol. 40, No. 1 size, molar pattern and dental formula (ig ci pe m3) rule out all North and Middle American bats except Promops centralis and Antrozous. Promops may be excluded by the quite different appearance of the labial surface of the coronoid region. Of the two species of Antrozous recognized by Orr (1954), A. bunkeri is distinctly larger than the Paraiso mandible. A. pallidus resembles it in all respects. The University of Michigan Museum of Zoology has six specimens from Tula, which were mentioned by Orr (1954). Sylvilagus floridanus.—Paraiso: one maxillary fragment of a young indi- vidual. Goodwin (1954) records the species from Gémez Farias, Pano Ayuctle and Chamal. Glaucomys volans.—Inferno: two palatal fragments, ten mandibles; Rancho del Cielo: one mandible; Paraiso: one mandible. From the dental formula (i: co py m3) these specimens are clearly referable to the Sciuridae, of which all northeastern Mexican species except Eutamias bulleri, E. dorsalis and Glau- comys volans are clearly too large. In Eutamias, however, the mandible is much less deep than in the Tamaulipas material. The latter bears a convincing resemblance to G. volans. The nearest locality from which the species had previously been obtained is Santa Barbarita in San Luis Potosi ( Dalquest, 1953). Liomys irroratus.—Paraiso: one maxillary fragment. Goodwin (1954) re- cords a series from Pano Ayuctle. Oryzomys alfaroi—tInferno: four maxillary fragments, one partial skull; Paraiso: three mandibles. Goodwin (1954) and Hooper (1953) have each recorded the species from Rancho del Cielo. R. (Reithrodontomys) megalotis——Inferno: one partial skull. Identification of this fragment is tentative. The species has already been recorded from Rancho del Cielo by both Goodwin (1954) and Hooper (1953). R. (Aporodon) mexicanus.—Inferno: five partial skulls; Rancho del Cielo: two partial skulls. The species has been recorded previously from Rancho del Cielo by Goodwin (1954) and Hooper (1953). Peromyscus boylei.—Inferno: two partial skulls, 15 maxillaries; Rancho del Cielo: one mandible. The species is recorded by Goodwin (1954) from both Rancho del Cielo and Rancho Viejo. Peromyscus pectoralis—Inferno: one partial skull, one maxillary. It has been recorded by Goodwin (1954) from both La Joya de Salas and 2 km. west of El Carrizo. Peromyscus ochraventer.—Inferno: one partial skull, six maxillaries. The species has been recorded from Rancho del Cielo by both Goodwin (1954) and Hooper (1953). Baiomys taylori—Paraiso: one mandible. Goodwin (1954) and Hooper (1953) have recorded it from Pano Ayuctle. Sigmodon hispidus.—Paraiso: one rostral half, ten maxillaries, two pre- maxillaries, three braincase elements, 16 mandibles. The species has been recorded from Pano Ayuctle by Goodwin (1954) and Hooper (1953). Neotoma angustapalata.—Inferno: four partial rostra, five maxillaries, eight 506 Feb., 1959 KOOPMAN AND MARTIN—MAMMALS OF EASTERN MEXICO 7 mandibles; Rancho del Cielo: one maxillary; Paraiso: one maxillary fragment, two premaxillaries, six mandibles. There is also a great deal of additional Neotoma material from Inferno that probably belongs here, but which has not been specifically identified. Both Goodwin (1954) and Hooper (1953) list specimens from Rancho del Cielo and El Pachon although, as Hooper points out, the precise status of N. angustapalata and its various southern Tamaulipas populations is far from clear. At the present time this name appears to be something of a “catch-all.” It is felt, however, that a revision should be based on entire specimens rather than on skeletal fragments. FAUNAL COMPARISONS AND THE STATUS OF GLAUCOMYS The identifications summarized in Table 1 represent total number of an- terior skull elements and not total number of individuals, which may be some- what less. Although such data do not lend themselves to close quantitative inspection, we feel that the faunas sampled near Inferno and Paraiso reveal important differences. Two quite different habitats, Cloud Forest and Tropical Evergreen Forest, are represented. It would be surprising if the faunas were qualitatively similar. Peromyscus, the dominant genus comprising 27 per cent of the Inferno deposits, is unrepresented at Paraiso. In turn, Sigmodon, which comprises 57 per cent of the material obtained at Paraiso, is absent from Inferno. Such a discrepancy may reflect an ecological shift in the dominant cricetine form. Other rather common species which appeared only in the Cloud Forest caves include: Marmosa mexicana (18%), Cryptotis mexicana (10%) and Reithrodontomys mexicanus (5%). One genus, Neotoma, occurs at both localities with a relatively constant frequency, 17-18 per cent. Within the Gomez Farias region the following are known only from their skeletal remains: Marmosa mexicana, Cryptotis pergracilis, Chilonycteris parnellii, Enchisthenes harti, Eptesicus fuscus, Lasiurus cinereus, Antrozous pallidus and Glaucomys volans. Presence of the latter is perhaps of greatest interest. In Middle America flying squirrels are very poorly known, presumably the result of their nocturnal and arboreal habits rather than an inherent scarcity. We are aware of ten other locality records between Chihuahua and Honduras, each represented by one or two specimens. In the Gémez Farias region remains of Glaucomys appeared at each cave locality, suggesting a general range through humid forest, both Cloud Forest and Tropical Evergreen Forest, between 420 and 1,320 meters. To our knowledge Glaucomys has not previously been collected in lowland tropical forests (below 1,000 meters). THE LOWLAND TROPICAL GRADIENT IN EASTERN MEXICO We might imagine a lowland tropical fauna to decline with increasing lati- tude at a rather regular rate. However, in reality the environment and fauna undergo a series of discrete changes, stepwise (see Fig. 1). In eastern Mexico four major tropical lowland vegetation types are represented. From south to north they terminate in the following sequence: Rainforest, Tropical Ever- 507 8 JOURNAL OF MAMMALOGY Vol. 40, No. 1 green Forest, Tropical Deciduous Forest and Thorn Forest (Leopold, 1950). Each terminus is marked by a steepening of the faunal gradient. In defining the lowland tropical fauna we have excluded those genera with distributional centers in temperate montane habitats or of limited lowland tropi- cal ranges, e.g., Idionycteris, Neotoma, Sciurus, Sigmodon and Baiomys. On the other hand, some of the species selected may range into montane habitats or reach temperate latitudes, such as Marmosa mexicana and Didelphis mar- supialis. In general the species listed in Table 2 are of wide distribution in lowland tropical America. Although they occupy tropical environments of the Mexican escarpment and coastal plain, we exclude Baiomys and Sigmodon because their phylogeny indicates a north temperate origin and in the case of Baiomys because it does not range extensively into Central America. Clearly the question of “tropicality” can be vexing. As one might expect the bats have much more extensive ranges than the small terrestrial mammals. The faunas of Trinidad and southern Tamaulipas share 18 species of bats, but none of rodents. EDWARDS EASTERN Sf ° t 24° e 10 30 40 VEGETATION NORTHERN LIMIT OF TROPICAL MAMMALS NUMBER OF TROPICAL SPECIES TYPE G@nyos NYOHL 1S3y¥04 NYOHL 20 Fic. 1.—Relationship between lowland tropical mammals and latitude in northeastern Mexico. Known range limits for 43 species listed in Table 2 are shown on the map. Major vegetation types are indicated at the right. Tropical Evergreen Forest is abbreviated to TEF. 508 Feb., 1959 KOOPMAN AND MARTIN—MAMMALS OF EASTERN MEXICO 9 The general relationship between vegetation, latitude and tropical fauna is shown on Fig. 1. In southern Tamaulipas a rapid “thinning” of tropical forms is evident. Between 23° and 24° north latitude the following 17 genera find their range limits: Philander, Marmosa, Chilonycteris, Pteronotus, Micro- nycteris, Macrotus, Glossophaga, Sturnira, Artibeus, Enchisthenes, Centurio, Natalus, Rhogeesa, Molossus, Heterogeomys, Eira and Mazama. At this latitude (24° north) the Tropical Deciduous Forest, well developed and widespread east of the Sierra de Tamaulipas and the Sierra Madre Oriental, disappears. Small, perhaps relict, stands of Cloud Forest and Tropical Evergreen Forest in the Gémez Farias region also enrich the environmental opportunity for tropical mammals. However, these habitats, especially the Tropical Evergreen Forest, are more extensive in southeastern San Luis Potosi and northern Veracruz. In this region seven genera terminate: Carollia, Tamandua, Coendou, Cuni- culus, Potos, Galictis and Ateles. Although the vegetation near Xilitla, San Luis Potosi, has been designated as Rainforest, it seems preferable to reserve that term for the more luxuriant forests of southern Veracruz with their short dry season. Lowland tropical forests near Xilitla appear taller and richer than those of southern Tamaulipas; however, the area has suffered a long history of intensive Huastecan agriculture. Almost certainly the primeval fauna of southeastern San Luis Potosi included a larger number of tropical genera at their northern limit. While we have not attempted to represent tropical distributions and plant formations south of San Luis Potosi, the following genera or subgenera approach their northern limit in southern Veracruz: Caluromys, Vampyrum, Rhynchiscus, Centronycteris, Mimon, Chrotopterus, Hylonycteris, Chiroderma, Alouatta, Tylomys, Dasyprocta, Tayassu, Tapirella and Jentinkia. Is there a relationship between these and the northern limit of Rainforest (see Leopold, 1950)? Extending from central Tamaulipas northward to Nuevo Leén and southern Texas is a rather barren Thorn Forest and Thorn Scrub. Gradually these arid habitats lose their tropical character as the Rio Grande Valley is approached. By comparison with plant formations to the south, this environment is poor in tropical fauna. The shift from tropical to temperate thorn scrub involves no sharp faunal boundary among the mammals. Oryzomys couesi and Liomys irroratus are among the forms reaching southern Texas. At this latitude the herpetological fauna includes such tropical genera as Coniophanes, Drymobius, Leptodeira, Smilisca and Hypopacus. However, among the reptiles and am- phibians, as well as the mammals, the greatest reduction in tropical fauna is found in southern Tamaulipas (Martin, 1958). DISCUSSION Although our analysis in confined to eastern Mexico, some interesting com- parisons can be made with the tropical biota of the Pacific Coast. Arid tropical vegetation and the genera Macrotus, Balantiopteryx, Chilonycteris, Pteronotus, Mormoops, Glossophaga, Desmodus, Natalus, Rhogeesa and Nasua extend far- 509 JOURNAL OF MAMMALOGY Vol. 40, No. 1 TABLE 2.—Northern limits of neotropical mammals LOCALITY AND APPROX. ELEV. REFERENCE SPECIES PRESENT San Luis Potost: A. Tamazunchale, 120 m. B. Xilitla and vicinity 630-1350 m. C. Rio Verde, 990 m. D. Valles, 75 m. E. El Salto, 660 m. Tamaulipas: F. Rancho del Cielo and vicinity, 1000-1320 m. Pano Ayuctle, 100 m. G. 2 km. W of El Carrizo, 800 m. H. Jaumave, 730 m. I. 10-16 mi. WSW Piedra, 400 m. J. 2 mi. S Victoria, 400 m. . 80 km. NW Victoria, 1000 m. . La Pesca, 10 m. . Rancho Santa Rosa, 260 m. . 8 mi. SW Padilla, 100 m. Nuevo Leén: O. 25 km. SW Linares, 700 m. P. 20 mi. NW General Teran, 300 m. Texas: Q. Hidalgo Co., 60 m. R. Raymondville, 30 m. Zeger wR Dalquest, 1953 Dalquest, 1953 Dalquest, 1953 Koopman, 1956 Dalquest, 1953 Goodwin, 1954 Hooper, 1953 present report Goodwin, 1954 Hooper, 1953 de la Torre, 1954 Baker, 1951 UMMZ specimens Anderson, 1956 Davis, 1951 Malaga-Alba, 1954 Anderson, 1956 Anderson, 1956 Lawrence, 1947 Malaga-Alba, 1954 Hooper, 1947 Blair, 1952b Blair, 1952b 560 Lael coal oe Al oad One co ee SOO OND UR bo NNNWNNWNWW SNSaseone 30. 31. 34. 35. OCOADAPR wh Tamandua tetradactyla . Sturnira ludovici Coendou mexicanum . Cuniculus paca . Potos flavus Galictis canaster Molossus major . Balantiopteryx plicata . Carollia perspicillata . Marmosa mexicana . Enchisthenes harti . Oryzomys alfaroi . Reithrodontomys (Aporodon) mexicanus . Mazama americana . Micronycteris megalotis . Sturnira lilium . Artibeus jamaicensis . A. lituratus . A. cinereus . Eira barbara . Philander opossum . Heterogeomys hispidus . Macrotus mexicanus . Chilonycteris parnellii . Glossophaga soricina . Centurio senex . Natalus mexicanus . Molossus rufus . Diphylla ecaudata Rhogeesa tumida Pteronotus davyi . Oryzomys melanotis . Desmodus rotundus . Oryzomys fulvescens Oryzomys couest Liomys irroratus Feb., 1959 KOOPMAN AND MARTIN—MAMMALS OF EASTERN MEXICO 11 TABLE 2.—Continued LOCALITY AND APPROX. ELEV. REFERENCE SPECIES PRESENT Coahuila and West Texas: Baker, 1956 36. Choeronycteris mexicana Miller and 37. Leptonycteris nivalis Kellogg, 1955 Edwards Plateau, Texas: Blair, 19524 38. Mormoops megalophylla Blair, 1952b 39. Nasua narica Eastern United States: Miller and 40. Dasypus novemcinctus Kellogg, 1955 41. Didelphis marsupialis ther north on the western side. On the other hand the humid tropical fauna and plant formations, e.g., Cloud Forest, Tropical Evergreen Forest and Rainforest, are absent or poorly represented on the Pacific slope north of Chiapas. As a general rule for those species or vicariant species occurring on both sides of Mexico, the arid tropical forms range farther north on the west, and the humid tropical forms farther north on the eastern side. This pattern is evident also in the distribution of lowland tropical birds, reptiles, insects, etc. Other than noting a rather close “fit,” it is beyond our purpose to explore the causal relationship between formation and fauna. In brief our conclusions may be summarized as follows: 1. The decline of the tropical fauna in eastern Mexico corresponds with the vegetation gradient. 2. Where the vegetation gradient steepens and a plant formation is lost, one finds a variety of tropical animals at their range limits. 3. In southern Tamaulipas the northern limit of many tropical mammals corresponds roughly to the boundary of Tropical Deciduous Forest. Contribu- ting to the rich tropical fauna of the Gomez Farias region are relict outposts of Tropical Evergreen Forest and Cloud Forest. 4. The problem of establishing a Nearctic-Neotropical faunal boundary in eastern Mexico can be approached realistically in terms of steps in an environ- mental gradient. ACKNOWLEDGMENTS First we wish to thank Dr. Byron E. Harrell for assistance in the field work. We are indebted to the Mammal Department of the American Museum of Natural History for use of their facilities including collections of comparative material. Mr. Sydney Anderson of the Museum of Natural History, University of Kansas, and Dr. William H. Burt, Museum of Zoology, University of Michigan, kindly advised us concerning specimens in their care. LITERATURE CITED ANDERSON, SYDNEY. 1956. Extensions of known ranges of Mexican bats. Univ. Kans. Publ. Mus. Nat. Hist., 9: 349-351. Baker, Rottriy H. 1951. Mammals from Tamaulipas, Mexico. Univ. Kans. Publ. Mus. Nat. Hist., 5: 207-218. 561 i, JOURNAL OF MAMMALOGY Vol. 40, No. 1 1956. Mammals of Coahuila, Mexico. Univ. Kans. Publ. Mus. Nat. Hist., 9: 125-335. Buair, W. FRANK. 1952a. Bats of the Edwards Plateau in Central Texas. Tex. Jour. Sci., 4: 95-98. 1952b. Mammals of the Tamaulipan Biotic Province in Texas. Tex. Jour. Sci., 4: 230-250. Da.QuEsT, WALTER W. 1953. Mammals of the Mexican State of San Luis Potosi. La. State Univ. Studies, No. 1: 1-112. Davis, Wiit1aM B. 1944. Notes on Mexican mammals. Jour. Mamm., 25: 370-403. 1951. Bat, Molossus nigricans, eaten by the rat snake, Elaphe laeta. Jour. Mamm., 32: 219. Goopwin, Greorce G. 1954. Mammals from Mexico collected by Marian Martin for the American Museum of Natural History. Amer. Mus. Novit., No. 1689: 1-16. Hooper, EMMeET T. 1947. Notes on Mexican mammals. Jour. Mamm., 28: 40-57. 1953. Notes on mammals of Tamaulipas, Mexico. Occ. Pap. Mus. Zool., Univ. Mich., No. 544: 1-12. Koopman, Kart F. 1955. A new subspecies of Chilonycteris from the West Indies and a discussion of the mammals of La Gonave. Jour. Mamm., 36: 109-113. 1956. Bats from San Luis Potosi with a new record for Balantiopteryx plicata. Jour. Mamm., 37: 547-548. LAWRENCE, BARBARA. 1947. A new race of Oryzomys from Tamaulipas. Proc. New England Zool. Club, 24: 101-103. LEopotp, A. STARKER. 1950. Vegetation zones of Mexico. Ecology, 31: 507-518. MALAGa-ALBA, AURELIO. 1954. Vampire bat as carrier of rabies. Amer. Jour. Public Health, 44: 909-918. Martin, Paut S. 1958. Herpetology and biogeography of the Gémez Farias region, Mexico. Misc. Publ. Mus. Zool., Univ. Mich. In press. Mier, Gerrit S., Jr. 1897. Revision of the North American bats of the family Vespertilionidae. N. Amer. Fauna 13: 1-155. AND REMINGTON KELLocc. 1955. List of North American Recent mammals. Bull. U.S. Nat. Mus., 205: 1-954. Orr, Rosert T. 1954. Natural history of the pallid bat, Antrozous pallidus (Le Conte). Proc. Calif. Acad. Sci., 28: 165-246. Torre, Luis pE LA. 1954. Bats from southern Tamaulipas, Mexico. Jour. Mamm., 35: 113-116. 1955. Bats from Guerrero, Jalisco, and Oaxaca, Mexico. Fieldiana: Zool., 37: 695-703. Dept. of Biology, Queens College, Flushing, New York and Institut de Biologie, Universite de Montreal, Montreal, Canada. Received August 6, 1957. 562 Reprinted for private circulation from THE AMERICAN NATURALIST, Vol. 105, No. 945, September-October 1971, pp. 467-478 Copyright © 1971 by the U ey of Chicago. All rights reserved. Printed in U. S. A. MAMMALS ON MOUNTAINTOPS: NONEQUILIBRIUM INSULAR BIOGEOGRAPHY JAMES H. Brown* Department of Zoology, University of California, Los Angeles, California 90024 INTRODUCTION MacArthur and Wilson (1963, 1967) have provided a theoretical model to account for variation in the diversity of species on islands. This model, which attributes the number of species on an island to an equilibrium be- tween rates of recurrent extinction and colonization, appears to account for the distribution of most kinds of animals and plants on oceanic islands. However, in addition to these islands, there are many other kinds of analo- gous habitats. Obvious examples are caves, desert oases, sphagnum bogs, and the boreal habitats of temperate and tropical mountaintops. It is of interest to ask whether the variables which determine the number of species on oceanic islands have similar effects on the biotas of other isolated habitats. For example, it has recently been shown that aquatic arthropods in caves (Culver 1970) and Andean birds in isolated paramo habitats (Vuilleumier 1970) are distributed as predicted by the equilibrium model of MacArthur and Wilson. The boreal mammals of the Great Basin of North America provide excellent material for testing the generality of the equilibrium model. Almost all of Nevada and adjacent areas of Utah and California are covered by a vast sea of sagebrush desert, interrupted at irregular intervals by isolated mountain ranges. The cool, mesic habitats characteristic of the higher elevations in these ranges contain an assemblage of mammalian species derived from the boreal faunas of the major mountain ranges to the east (Rocky Mountains) and west (Sierra Nevada). Thanks largely to the work of Hall (1946), Durrant (1952), and Grinnell (1933), mammalian distributions within the Great Basin are documented quite thoroughly. I have used the work of these authors and data accumulated during 3 summers of my own field work in the Great Basin to produce the following analysis. I shall show that the diversity and distribution of small mammals on the montane islands cannot be explained in terms of an equilibrium between colonization and extinction. Boreal mammals reached all of the islands during the Pleistocene; since then there have been extinctions but no colonizations. * Present address: Department of Biology, University of Utah, Salt Lake City, Utah 84112. 467 563 468 THE AMERICAN NATURALIST METHODS The Montane Islands Because mountains do not have discrete boundaries, islands were defined by operational criteria applied to topographic maps (U.S. Geological Survey maps of the states; scale 1: 500,000). A mountain range was considered an island if it contained at least one peak higher than 10,000 feet and was isolated from all other highland areas by a valley at least 5 miles across below an elevation 7,500 feet. This altitude corresponds approximately to the lower border of montane pifon-juniper woodland. Application of the above criteria defined 17 islands (fig. 1; table 1) which lie in a sea, the Great Basin, between two mainlands, the Sierra Nevada to the west and the central mountains of Utah (a part of the Rocky Mountains) to the east. The sizes (areas) of the islands and the distances between islands and between islands and mainlands have been determined from the topographic maps. The Boreal Mammals As with the montane islands, the mammals restricted in range to the higher altitudes must be defined somewhat arbitrarily. I have selected those A Fic. 1.—The Great Basin, with the montane islands lying between the Sierra Nevada (left) and Rocky Mountains (right). The shaded islands were used for the present analysis and are identified in table 1. The two unshaded islands were not used because they lie on the northern perimeter of the Great Basin and their faunas are poorly known. 564 MAMMALS ON MOUNTAINTOPS 469 TABLE 1 CHARACTERISTICS OF THE MOUNTAIN RANGES CONSIDERED AS ISLANDS Boreal Area above Highest Highest Nearest Nearest Mammal 7,500 Feet Peak Pass* Islandt Mainland Species Mountain Range (Sq Miles) (Ft) (Ft) (Miles) (Miles) (NV) 1. White-Inyo ..... 738 14,242 7,000 82 10 9 Qa Panamanity arvensis 47 11,045 5,500 19 52 1 Se ODL Otay sicieraareiete 125 11,918 3,500 108 125 3 4 Loiyabews cs ae. s 684 11,353 6,000 iste 110 12 5. Toquima-Monitor 1,178 11,949 7,000 9 114 9 oe Comite! sbogese cee 150 11,298 7,000 17 138 3 i. Diamond! Pca. « 159 10,614 7,000 7 190 4, 8. Roberts Creek ... 52 10,133 7,000 22 216 4 OM RUDYe awaoe see 364 11,387 6,000 Seve 173 12 NOS DEUCE Weer ace ar 49 10,262 6,500 12 156 3 11. White Pine ..... 262 11,188 7,000 43 150 6 12. Schell Creek-Egan 1,020 11,883 7,000 11 114 7 NSy, USM a aes oa 12 10,704 5,000 33 114 2 14. Deep Creek ..... 223 12,101 7,000 9 104 6 15s enaker o.). .ciecee 417 13,063 7,000 76 89 8 1G, Stansbury... es. 56 11,031 6,000 4 39 a ily Ofotiadd Aan aas 82 10,704 5,500 88 19 5 * Elevation of the highest pass separating the island from the mainland or from another island with more species. +t Distance to the nearest island with more species. No distance is given for the Toiyabe and Ruby Mountains because no other islands have more species. species that occur only at high elevations in the Rockies and Sierra Nevada and are unlikely to be found below 7,500 feet at the latitudes of the Great Basin. I have excluded large carnivores and ungulates from the analysis because their distributions were drastically altered by human activity be- fore accurate records were kept. I have also ignored the bats because their distributions are very poorly known and because their dispersal by flight introduces a completely new variable that could only complicate the present discussion. After these omissions, there remain 15 species of mammals (table 2) which occur in the Sierra Nevada and Rocky Mountains and on at least one of the montane islands of the Great Basin. All of these species occur in pifon-juniper, meadow, or riparian habitats. A striking feature of the mammalian faunas of the isolated peaks is the absence of those species which are restricted to dense forests of yellow pine, spruce, and fir in the Sierra Nevada and Rocky Mountains. None of these species, which include Martes americana, Aplodontia rufa, Eutamias speciosus, Tamiasciurus hudsonicus, T. douglasi, Glaucomys sabrinus, Clethrionomys gapperi, and Lepus americanus, are found on any of the isolated mountain ranges of the Great Basin, even though some of the large islands have large areas of ap- parently suitable habitat. However, the well-developed coniferous forests on the large islands have a good sample of the avian species characteristic of these habitats on the mainlands. Records of occurrence are taken from the literature (Hall 1946; Hall and Kelson 1959; Durrant 1952; Durrant, Lee, and Hansen 1955; Grinnell 1933) and from my own observations which concentrated on the small mountain ranges. Undoubtedly, there are a few errors of omission that will 565 THE AMERICAN NATURALIST 470 GaLIgVHNT JLT SANVIST ‘ON IVLOL "SNULLQUN “TT YAIM Sotoodsiedns & SWAIOZT YOTYM “OTMapUS Uv “Wwawjnd sDLWYIN| St Sotoods oy} gE PULI[ST UC } ‘supi6va “gS YYIM sotoedsiodns & SUIIOJ YOIYyM ‘WIOF ulvyuNOP, AYO ®B ‘snunasqo La1og St Soteds 94} JT PURIST UO , : a x eG ee | Ge) eB se FOR oe Xe XOX ce anes x x sie eX: x x xX So XX oc Xo Xe ar = So eX So, x ee Be se} x a a as = “5 a eric a = oO O @) oT OE: l 10 100 1000 10,000 BODY WEIGHT (GRAMS) Fic. 3.—Frequeney of occurrence on the montane islands of species of boreal mammals plotted against their body weight; shaded cireles represent herbivores which are found in most habitats, unshaded circles indicate herbivores with specialized habitat requirements, triangles denote carnivores. The abbreviations are of species names which can be identified by reference to table 2. ing, MacArthur and Wilson (1963) have proposed a model which represents the number of species on an island as a dynamie equilibrium between rates of colonization and extinction. The effect of recurrent colonization on spe- cies diversity is usually assessed by expressing the number of species on an island as a percentage of the number present in an area of the same size on the mainland and plotting this percentage saturation against the dis- tance to the nearest mainland. When this is done for the montane mammals of the Great Basin, no relationship (r = .005) is observed (fig. 4). This is in marked contrast to the inverse correlation predicted by the equilibrium model and observed for various groups of organisms on oceanic islands (MacArthur and Wilson 1967) and for birds on montane islands (Vuil- leumier 1970). Before concluding that recurrent colonization has not been a significant factor in determining the diversity of mammals on the montane islands, it is necessary to exclude three alternative explanations: (1) Differences in habitat between islands may be sufficiently great to obscure the distance effect (see Diamond 1969). The montane islands of the Great Basin have similar vegetation, climate, and geomorphology; but they differ somewhat in elevation, which may affect the amount and diversity of boreal habitats 569 474 THE AMERICAN NATURALIST PER CENT SATURATION 0) 50 fete) I50 200 DISTANCE FROM MAINLAND (MILES) Fic. 4.—Percentage of faunal saturation plotted against distance from the Sierra Nevada or Rocky Mountains, whichever is nearer, for the 17 montane islands listed in table 1. Percentage of saturation is defined in the text. in a manner different from insular area. (2) The islands may acquire most of their mammalian colonists from other islands (by a stepping-stone pro- cess) rather than directly from the nearest mainland, so that distance between islands might be an important variable affecting immigration. If this is so, the nearest island with more species is the most likely source of colonists if it is nearer than the closest mainland. (3) The effectiveness of the desert barriers surrounding the islands rather than the distance between mountains may be the most important variable influencing the rate of colonization. If this is true, the altitude of the highest pass should be the best measure available of the severity of the climatic and habitat barriers which separate the mountain ranges. The possibility that any of these three explanations may account for some of the variability in insular-species diversity and provide evidence of the effects of immigration can be evaluated by subjecting the data in table 1 to stepwise multiple regression analysis. The results of such analysis using a linear model are shown in table 3. Again it is apparent that the number of mammalian species inhabiting an island is closely related to insular area, although the correlation is not as good as when a logarithmic model is used. Neither elevation of the highest peak nor any of the three variables (dis- tance from nearest mainland, distance from nearest mountain with more species, elevation of highest intervening pass) which might be expected to 570 MAMMALS ON MOUNTAINTOPS 475 TABLE 3 INFLUENCE OF SEVERAL VARIABLES ON THE NUMBER OF SPECIES OF SMALL MAMMALS INHABITING MONTANE ISLANDS IN THE GREAT BASIN ANALYZED BY STEPWISE MULTIPLE REGRESSION USING LINEAR MODEL® Contribution Order Entered Variable to R2 F Value in Equation PAST Geile, WiMatteouapecaue iol eis erekorotele cecveree 49421 14.65* aL phestepeadke Sic. cite setetec< .00006 0.32 2 Nearest mainland ............. .00042 0.83 3 Nearest island) ~] ++ “ ++ ++ + + ++ ++ a 591 TROPHIC COMPARISON OF BATS TABLE 10. (Continued ) GENERA NEOT NEA Scotophilus* Otonycteris* Lasiurus* + Barbastella* Plecotus* + Euderma* Miniopterus* Murina* Harpiocephalus* Kerivoula* Lamingtona* Nyctophilus* Pharotis* Tomopeas* + Mystacina* T adarida* Otomops* Neoplatymops* + Sauromys* Platymops* Myopterus* Molossops* Eumops* Promops* Molossus* Cheiromeles* 8.8 ++ oh -- ede oi ++i Total for region 43.6 75.4 teen of the 26 genera in Table 11 are Neotropical. Several groups of bats may be used as illustrations of convergence. The Old World Tropical Megadermatidae seem to be the ecological equivalents of several genera of New World carnivorous Phy]l- lostomatinae. Fish-eating is practiced by different spe- cies in each of the six regions. Noctilio leporinus is the Neotropical representative of this role. Myotis vivesi occurs in the Nearctic region. Palearctic members in- clude Myotis daubentoni and M. macro- dactylus (Findley, 1972). Megaderma is an occasional fish-eater in the Oriental and Australian regions. Myotis accounts for the .3 value listed for the Ethiopian region, even though none of the six species are definitely known to fish. Blood feeding is a highly specialized FAUNAL REGION PALE ETHIO ORIENT AUST “- ~ - + + ~ + + + - ~ as - ~ - = a “ + ~ - -|- + + + e 133 + + ~ ~ is + + + 84.0 65.8 60.5 48.4 role found only in the Desmodontinae, a subfamily of the Neotropical Phyllosto- matidae. The absence of this trait in other regions is difficult to explain, since the Neotropical region seemingly has _ little more to offer in the way of host animals than other regions. It may be that this most specialized role has only appeared once due to the normal selective rigors which attend extreme specialization. Foliage gleaning is the most evenly dis- tributed food habit in all of the regions. Foliage gleaning bats have a suite of mor- phological and behavioral characters which go along with this feeding behavior, in- cluding large ears, broad wings, and a slow, maneuverable flight. Tonatia and some species of Micronycterus typify this pattern in the Neotropical region. The Nearctic region has Antrozous, Plecotus, and Myotis evotis, M. auriculus, and M. 592 26 SYSTEMATIC ZOOLOGY TasLe 11. GENERA SPECIALIZING (*) AND/OR CONTRIBUTING MAJOR AMOUNTS TO Frugivorous Trophic Role (6). Plus symbols (+) as in Table 9. FAUNAL REGION a 2 oe Se a Be ne ee ee ee ee ee GENERA NEOT NEA PALE ETHIO ORIENT AUST Eidolon* + Rousettus* a + Myonycteris* oe Boneia* Pteropus* 4.3 Acerodon* Neopteryx* Pteralopex* Styloctenium* Dobsonia* Harpionycteris* Plerotes* Hypsignathus* Epomops* Epomophorus* Micropteropus Scotonycteris* Casinycteris* Cynopterus* Megaerops* Ptenochirus* Dyacopterus* Chironax* Thoopterus* Sphaerias* Balionycteris* Aethalops* Penthetor* Haplonycteris* Nyctimene* Paranyctimene* Macroglossus* Syconycteris* Melonycteris* Notopteris* Micronycteris* Macrotus Tonatia* Anoura* Choeronycteris Leptonycteris Carollia* Rhinophylla* Sturnira* Uroderma* Vampyrops* Vampyrodes* Vampyressa* Chiroderma* Ectophylla* Enchisthenes* Artibeus* Ardops* + + a ee) wo +++ 44% 23.8 batt ++4j + +t4+4+4+t+4+4+4+4+44+ ++4++4++ ++++++++ (ey) Sas uw +H++t++44+ 593 TROPHIC COMPARISON OF BATS 27 TABLE 11. (Continued) GENERA Phyllops* Ariteus* Stenoderma* Pygoderma* Ametrida* Sphaeronycteris* Centurio* NEOT NEA +4++4++4+44 bo Total for region 30. 1.0 keenii. In the Palearctic region, Hipposide- ros, Rhinolophus, and several species of Myotis (e.g., bechsteini, emarginatus) fill this role. Aerial insectivores are common in all regions, and it might be better to view this as a basic feeding pattern rather than one FAUNAL REGION PALE ETHIO ORIENT AUST a 13.8 19.5 35.1 of convergence. The family Molossidae is found in all of the tropical regions and is composed entirely of aerial insectivores. The molossid genus Tadarida occurs in all six regions. The family Vespertilioni- dae has four genera (Myotis, Pipistrellus, Eptesicus, and Nyctecieus) which are cos- TABLE 12. GENERA SPECIALIZING (*) AND/OR CONTRIBUTING MAJOR AMOUNTS TO Nectarivorous Tro- phic Role (7). Plus symbols (+) as in Table 9. FAUNAL REGION GENERA NEOT NEA Rousettus* Pteropus Dobsonia Epomophorus* Nanonycteris* Eonycteris* Megaloglossus* Macroglossus* Syconycteris* Melonycteris* Notopteris* Glossophaga* Lionycteris* Lonchophylla* Platalina* Monophyllus* Anoura* Scleronycteris* Hylonycteris* Choeroniscus* Choeronycteris* Leptonycteris* Lichonycteris* Brachyphylla* Erophylla* Phyllonycteris* — t++++E4+4+ _ oo 1.9 +4+4+4++4+i re to Total for region 1 3.8 PALE ETHIO ORIENT AUST 7 8 6 oF a 9 2.6 + @ 2.2 + 11 a A + 1.0 1.0 + 7 5.5 3.5 6.4 594 28 mopolitan and all are primarily aerial in- sectivores. The monotypic Myzopodidae and Thyropteridae are specialists in this role in the Ethiopian and Neotropical re- gions, respectively. The Neotropical re- gion also has the families Furipteridae, Natalidae, and Mormoopidae, which are all aerial insectivores. The Emballonuridae, found in every region except the Nearctic, contains 12 genera which are exclusively aerial insectivores. In short, aerial insecti- vores are the most important component of every region. Frugivorous types are essentially limited to the tropical areas and are best repre- sented by the Pteropodidae in the Old World and the Phyllostomatidae in the New World. Nectarivorous bats are also essentially tropical and are mainly members of the above two groups. The subfamilies Glos- sophaginae and Phyllonycterinae of the Neotropical Phyllostomatidae have special- ized for this role, as have several genera of the pteropodid subfamily Macroglossinae in the Oriental, Ethiopian, and Australian regions. CONCLUSIONS 1. Additional study directed towards elucidation of food habits of bats is a necessary prerequisite to further studies of this sort. 2. The most important trophic role of bats is aerial insectivory, followed by frugivory, foliage gleaning, nectarivory, piscivory, carnivory, and sanguinivory. 3. The tropical faunal regions support a broader base of trophic roles than do the temperate regions. 4. Taxonomic zoogeographic analysis shows a direct correlation between dis- tance and similarity of faunal regions, while a trophic role approach emphi- sizes ecological similarity between major climatic areas, rather than dis- tance. 5. The lack of correlation between tax- onomic and trophic approaches to zoo- geography points up the pitfalls facing SYSTEMATIC ZOOLOGY a taxonomist dealing with suites of characters which may be influenced by trophic roles. 6. While the vagaries of historical caprice may dictate distributional contiguity, functional niches will be more likely controlled by environmental conditions. ACKNOWLEDGMENTS Pat Mehlhop, Ron Pine and Hank Setzer contributed valuable suggestions on drafts of the manuscript. I am grateful to Karl Koopman, both for his painstaking work in summarizing bat distributions and for his helpful criticism of the manuscript, even though he retains grave misgivings about the quantification of poorly known variables. REFERENCES ALLEN, G. M. 1939. Bats. Harvard Univ. Press, Cambridge, x + 368 pp. AraTA, A. A., J. B. VAUGHN, AND M. E. THOMAS. 1967. Food habits of certain Colombian bats. J. Mamm. 48:653-655. Barsour, R. W., anp W. H. Davis. 1969. Bats of America. Univ. Press Kentucky, Lexington. 286 pp. BoreLL, A. E. 1942. Feeding habit of the pallid bat. J. Mamm. 23:337. BrosseT, A., AND C. D. DEBOUTTEVILLE. 1966. Le regime alimentaire du Daubenton, Myotis daubentoni. Mammalia 30:247-251. CarvaLHo, C. T. 1961. Sobre los _habitos alimentares de _ phillostomideos (Mammalia, Chiroptera). Rev. Biol. Trop. 9:53-60. ConsTANTINE, D. G. 1966. New bat locality records from Oaxaca, Arizona and Colorado. J. Mamm. 47:125—126. DaruincTon, P. J., Jr. 1957. Zoogeography: The geographical distribution of animals. John Wiley and Sons, Ltd. London. Davis, W. B., D. C. CARTER, AND R. H. PINE. 1964. Noteworthy records of Mexican and Central American bats. J. Mamm. 45:375-387. Dunn, L. 1933. Observations on the camivo- rous habits of the spearnosed bat, Phyllostomus hastatus panamensis Allen in Panama. J. Mamm. 14:188-189. Dwyer, P. D. 1962. Studies on the two New Zealand bats. Zool. Publ. Victoria Univ., Wel- lington 28:1-28. FINDLEY, J. S. 1972. Phenetic relationships among bats of the genus Myotis. Syst. Zool. 21: 31-52. FLEMING, T. H., E. T. Hooper, anv D. E. WiL- 595 TROPHIC COMPARISON OF BATS son. 1972. Three Central American bat com- munities: structure, reproductive cycles and movement patterns. Ecology 53:555-569. GoopwIn, G. G., AND A. M. GREENHALL. 1961. A review of the bats of Trinidad and Tobago. Bull. Amer. Mus. Nat. Hist. 122:191-301. GREENHALL, A. M. 1966. Oranges eaten by Spear-nosed bats. J. Mamm. 47:125. GREENHALL, A. M. 1968. Notes on the behav- ior of the false vampire bat. J. Mamm. 49:337— 340. GRINNELL, H. W. 1918. A synopsis of the bats of California. Univ. Calif. Publ. Zool. 17:223- 404. Hatt, R. T. 1923. Food habits of the Pacific pallid bat. J. Mamm. 4:260-261. HOFFMEISTER, D. F., AND W. W. GoopPASTER. The mammals of the Huachuca Mountains, southeastern Arizona. Illinois Biol. Mongr. 24: 1-152. Hooper, E. T., anp J. H. Brown. 1968. For- aging and breeding in two sympatric species of Neotropical bats, genus Noctilio. J. Mamm. 49: 310-312. Howe .t, A. B. 1919. Some Californian experi- ences with bat roosts. J. Mamm. 1:169-177. Huey, L. M. 1925. Food of the California leaf- nose bat. J. Mamm. 6:196—197. JEANNE, R. L. 1970. Note on a bat (Phyl- loderma stenops) preying upon the brood of a social wasp. Science 51:624—625. KoopMan, K. F. 1970. Zoogeography of bats. In About Bats. Southern Methodist University Press. Dallas pp. 29-50. KoopMAN, K. F., anp J. K. Jones, Jr. 1970. Classification of bats. In About Bats. Southern Methodist University Press. Dallas pp. 22-28. Len, M. R. 1972. A trophic comparison of avi- faunas. Syst. Zool. 21:135—-150. Lim, B. L. 1966. Abundance and distribution of Malaysian bats in different ecological habi- tats. Fed. Mus. J., 11:61-76. Lim, B. L. 1970. Food habits and _ breeding cycle of the Malayasian fruit eating bat, Cynopterus brachyotis. J. Mamm, 51:174-177. 29 McNas, B. 1971. The structure of tropical bat faunas. Ecology 52:352-358. Mepway, L. 1967. A bat-eating bat Megaderma lyra Geoffroy. Malayan Nature J. 20:107-110. Orr, R. T. 1954. Natural history of the pallid bat, Antrozous pallidus (Le Conte). Proc. Calif. Acad. Sci. 28:165-246. Poutton, E. B. 1929. British insectivorous bats and their prey. Proc. Zool. Soc. London 1929: 277-303. Pine, R. H. 1969. Stomach contents of a free- tailed bat, Molossus ater. J. Mamm. 50:162. Ross, A. 1961. Notes on food habits of bats. J. Mamm. 42:66-71. Ross, A. 1967. Ecological aspects of the food habits of North American insectivorous bats. Proc. West. Found Vert. Zool. 1:205-264. Ryserc, O. 1947. Bats and bat parasites. Natur. Stockholm xvi + 329 pp. SHERMAN, H. B. 1935. Food habits of the Seminole bat. J. Mamm. 16:224. Sirva, T. G., AND R. H. Pine. 1969. Morpho- logical and behavioral evidence for the relation- ships between the bat genus Brachyphylla and the Phyllonycterinae. Biotropica 1:10-19. SrorerR, T. F. 1926. Bats, bat towers mosquitoes. J. Mamm. 7:85-90. Tan, K. B. 1965. Stomach contents of some Borneo mammals. Sarawak Mus. J. 12:373-385. TurtLe, M.D. 1967. Predation by Chrotopterus auritus on Geckos. J. Mamm. 48:319. TutrtLe, M.D. 1968. Feeding habits of Artibeus jamaicensis. J. Mamm. 49:787. VALDEZ, R., AND R. K. LaVaut. 1971. Records of bats from Honduras and Nicaragua. J. Mamm. 52:247-250. Wa.ker, E. P. 1968. Mammals of the world (2nd ed.) Vol. I, pp. 182-392. John Hopkins Press, Baltimore. Wiuson, D. E. 1971. Food habits of Micro- nycteris hirsuta (Chiroptera: Phyllostomatidae). Mammalia 35:107-110. and Manuscript received August, 1972 596 A Numerical Analysis of the Distributional Patterns of North American Mammals. IL. Re-evaluation of the Provinces EDWIN M. HAGMEIER Abstract In an earlier paper, numerical techniques were developed and used to analyze distribu- tion patterns of the native terrestrial mammals of North America. An error in method is here corrected, indicating that 35 provinces, 13 superprovinces, four subregions, and one region may be recognized. The methods used are relatively objective, quantitative, and suited to computerization. Introduction In an earlier paper (Hagmeier and Stults, 1964, hereafter referred to as H & S), quan- titative and relatively objective methods were used to demonstrate that (1) the range limits of North American terrestrial mammals are grouped, (2) that as a result it was possible to delimit geographic re- gions of faunistic homogeneity which were termed mammal provinces, and (3) that such provinces could be useful in the analy- sis of other zoogeographic phenomena. This paper is concerned with the recal- culation of some of the data of the second item above. It was assumed in our earlier paper (H & S) that several of the large provinces of the northern half of the con- tinent required further analysis. On initia- tion of this analysis, it became apparent that an error in method had been made which required correction. As a consequence of the correction, the number of North Ameri- can mammal provinces is here increased from 22 to 35, two of which are of uncertain status. The general philosophy, methodology, and conclusions reached in our earlier paper (H & S) do not differ from those arrived at here, and the earlier paper should be referred to for accounts of these. The ma- terial given here, since it is essentially re- visionary, is presented in as brief a form as possible. Because of the changes reported here, the analysis of mammal areas given in H &S (p. 141-146 and Figs. 6c-8d) needs revision, and this revision will form the sub- ject of a future paper. Since submission of our earlier paper (H & S), Simpson (1964) has considered variation in abun- dance of species of North American mam- mals in a superior manner, and his work should be referred to for a treatment of the subject. Derivation of Provinces In our earlier paper (H & S), the ranges of all 242 species of native terrestrial North American mammals were converted into a model, first by separately computing the percentage of species and genera whose ranges ended within blocks 50 miles by 50 miles throughout the continent (each such value was called Index of Faunistic Change, or IFC), second by plotting species and genus IFCs on maps of North America, and third by fitting isarithms. The species IFC map resulting was given as H & S, Figure 1. Low IFC values indicated faunistic homogeneity, and regions characterized by such values were termed primary areas. 279 597 280 SYSTEMATIC ZOOLOGY Fic. 1. Twenty-four of these were identified through examination of IFC maps of both species and genus and species checklists of each were prepared (H & S, Table 2). The per- centage of species common to all combina- tions of pairs of provinces (Coefficients of Community, or CCs, Jaccard, 1902) were then computed. CCs were then subjected to cluster analysis using the weighted pair- group method, and simple averages (Sokal and Sneath, 1963:180-184, 304-312; H & S: 132, 137), and drawn up in the form of a dendrogram (H&S, Fig. 5). Primary areas pooled at a mean CC level lower than 62.5% were termed mammal provinces, those pool- Eighty-six primary areas derived through examination of IFC Map (H & S, Fig. 1). ing at below 39% were termed mammal superprovinces, those below 22.5%, mam- mal subregions, those below 8% as mammal regions. The basis of our error lay in the fact that we attempted to identify only the 24 North American mammal areas corresponding to those described by Kendeigh (1961) in his modification of Dice’s (1943) scheme of biotic provinces. This error became appar- ent only when subsequent analysis of parts of certain of these provinces showed that the parts in some cases merited full prov- ince status. The correction made and reported here 598 281 DISTRIBUTION OF NORTH AMERICAN MAMMALS x xX KX xX x xX x xX x x x x xX X SE FE CE SE » OOs 5 p = O wo Se PF Ss © 9 #. 3 op 8 Bb Se eg = 5 E. 3 al oO S ueoyeWF ues x xX X € ueTqUIy SAO PE OR OS x x x x 6% 8G LZ 9G GS ZER EE 5% 28 ¢ Bs Gs o 8 & 8 tee B65 § 5 i=} UvISoWINV a ise) a ueiquin[od Sale uviuRIsSMo'y uexa J, x x i=} a uedrjnewe J, op) onl ueMooleg x ioe) Lal URIURMIYOIEYSES x xX uvsuey x xX x i) a UBIIDANOOUP A x x x UEPLIOION & uvluewoyWy, © x x x x xX X X X x x xX xX xX XK X x &X x xX X x KX KX KX KK XK XK XK MLHLH9MIG F EC MOUS I ge up =e lets oGBreé sg en FS BB ae Veep See hss p 2 &® ® esp Be F ae es 6 8 Secs = p 8 5 o 5° gE 5 3 snauonbp ° nuognpnp ° yop SYDUOI}ISUD.L} * snuppiso}f * siuysnjpod ° 1UDULY IDG * sisuaoyppr snsopajhs sdaguiud “OQ S14D]]09 DUOJOYID snyourgwmaaou sndhsvq DID}S1LI DANgipuoy snoayonbp sndojv9g 1anasg sdojpasp.i0g upuasuno} ‘Ss SNUDULI}D] *S smiip4o snupdpaIs usqqia snyIi4jo1na 1ps0fNd49 X91L0S01}0 N paspd s14zojdhsy Dpnvoiaasq DUD) g thoy xaLoso1n PW MUWDLLLIU * tas pliqno.y * ivdszp ° SNIVYILD * snaun{ ° 1aupuag * siugsrypd * snupu * supidpva * SLLJSOMBUO] * snasau1d XAL0S sypnidnsipwu s1ydjapid NNNNNNHNAN ANNNNNNNANN 599 SYSTEMATIC ZOOLOGY iT) se] x ise] co se] uelqrid URTULOFTTeD UvIUIPIeUIeg UBS x x xx x x SnyDauIwarap1s} *S x KEK KEM OX SHON PUL Ss x snupiquinjoo ‘S x x idulpjaq °S x SNYDULID *S x x NUOSPLDYILL *S upuasumo} snjrydousads sninona) ‘VW usiipy snjrydowadsommy x x x DIDAYNDI *“W x x x stiquaaranpf * x x xX x xX X X x XDUOUL DIOUWLD WG snuLiquin * snuijutupund * Xx snsoizads * Xx snypjnopunsponb * Syponasauyo * x snpnooifns * snqyoypraiaponb * SY]DSLOp * x TUDILLOUL * x aDULOUOS * upuasuno} ‘7 x x x snuaowD "7 SNUUIUL “FT snuidjp sprupjng] x SNIDIAIS SOILD J, x x xX pint mnyuopojdy x wuaypD "'T 1psDyjyo3 “| SNNULO{YDI “"T upuasuno} “"T SNIUYIID “'T snupoiiaup sndaT xX xX XxX K X x FARRAR x x x x x x x xX XX x x x X KX KX KX XK XK Xn Oe x x xX x X x x x x x x x x x x XX x x XxX KX X x x x x 2 a uvowrysy “gl ueAesuyQ MLaL AI MI a ~ Ll ise) 1 Q 1 | e Lol i=) aa s uvraryow of uvayep ueg uenuin § ueruoyearn & uvwidey & uetumbe x = ue1ouos & ueqeqrey xt ueIsoweyy A ice) ueiquinjogn a a uelurIsMmoyT A uexeal, & uedijnewe J, = ueluoo[eg eZ ce) ei Kt Le | o ueIuI[OIeD) auerounl[yT uviueyseal[V ueIIaIS DE PLO UuLEy UBIUOZIIOC, ueIIdANOoUR A uepelojo)y & | xX uelurjwuopF © | X ueIpeUuRy "AA uvipeuey ‘Wy ueuospny “y uerluospny ‘A uevluoyN_ 0] xX uelneay ueyse[y | xX Xx UvOUWIAST “A ULIUBMIYOJCASES 282 (‘panuyjuon) ‘T aTavy 600 283 DISTRIBUTION OF NORTH AMERICAN MAMMALS x xX XK X x x x wD ioe) Ss (56) oD se] aQ o uelqriq ULIULIOFTTED) uvIALYO/, URIUIPIeuleg UBS al o So ise] uvojepy ues uenurg op) a uvruoyRaeNn oe] a uvruideyy bt a uviuinbe x Se) a wD nN uriqeqrey ~ a uvIsoWwayy se] AQ Q i uerquinjoD uvlueIstno’y urxay, a x XxX x X uedrpneule y, x o>) uvuo jeg - ioe) eS UBIUBMIYOeASeS uvsuey Ke) ol uelulporesy w a ~~ Lal se] eo a al OCT Tl uevrlueysel[V ue ppoquinyy (‘panu1juoy ) fo qo ueIUOSZIIC) x xX KX X XK X Cc = S | bs i] - ie o Ss © UBIIDANOOUR A uepeiojon © uviuewuop © uvIpeUury “A uvipeury “y uvruospnyy “y ueluospnyy “AA ueluoyNn_ 19 BECUCKAD x snanif ‘d VUDILLIUL * J suagsaan}f *d snyp1ospf snyyous01ag sdoupjspo shwoasojDLy syjauid *r) snyouossad "+ SM1LIDUALD *©) smupsing shuoary snioaiqjng * I, sapiod)n} * snuiiqun shwowoy I SNU1LGDS “5 supjoa shwoonp]y) uspjanop * I SNQWUOSpNYy SNINLISDLWD J SISUDUOZILD * ayovdp ° aa * Huaqn ° snastiia * SISUBUNJOLDI SNLNIIS quosiuuns "9D suapiaipd * 9) sningong] ‘9D snuniaiaopn) shuouhy SyD19}0] * sysuaaDyou * snpnpo1jaia} * thayoaag ° snyosa1sva * Muyyudds ° pwosojids * snupoixau * NANnNnNNN NNANNNNANN ueynay ueyse[y ° 3 a UBOUITYAST “AA OE OCS Sel a uvAesuyQ 601 SYSTEMATIC ZOOLOGY 284 x x x oe tae Re ae x x ie x x x & x x me x xx x x pa a4 x x x x ” x rs eM x x SE PE CE ZE LE OF oO Oo 2 woe BB ESS § ae CO) eee Ser 5B 2p e-P > Sete 3 cs m 5 e B i=} 8 Ile uemoyearn x X ice) fs] uviudeyy x xX xX ré a uviumbex x ce) nN ue1ouo0sg w aQ uriqeqrey ueIsSOuUlOHYy x XX X ~ nN KK ROX KR KK Xx KX x x x x £S GS Sats ae 5B x x xX KK XM XK x x xX X x IZ 0G 61T SI LI OT ST FI ET GI SOP PR OR Ee & Be oF 2388 @3 5 BE eS Be ees Be CS a ke i=} 3 5 p 5 5 5, 5 (‘panu1juoy ) cal — uvIUOZII9 x xX KX KX KX KX KK XK X snpui49 snoshiwosag suaosaqynf “Yy sLuquaaians "Y SIjO]DBaW "Yy synuny “Yy snupjuow shwojuopo.ypnay stuysnjod shuozhi 5 5 ueAesuyQ 602 285 DISTRIBUTION OF NORTH AMERICAN MAMMALS x xX xX X x xX XK XK XK X x NC snpnonduo] *g pjonaps ‘J sadiqp ‘dg Smpautsazur shwoouayd sypyuap1990 *D waddpa *y snquyns shuouo1sy}a19 Dalgutd * NI sadiasn{ *N DUDIIXOUL * NJ tsuaydays *N opida] *N pnsiqD “N sndosovu * NN puppiLopf{ DW0}0AN snyjDUus0.1yI0 *S SNUMULUL *S snpids1y uopowsis snpit4o} "OC lajspd0onay shwoyouc 110] hp} shwowg snuppi1ojf “J x myoune ° snynspu * vant} * syjp10jIad ° 1ajfiog snutdfisso3 ° sndoong ° snjouonod * snyojnaiupu TULDILLOUL Sna1wWasa * SsnqUsofyyva * x XXX xX x xX x X X eG mM KX MK KR MK RN NX Wis Wi ~~ ~~ ~~ ~~ uUPIUIpIeuleg UES x o urged URTUIOFTLD oD (S] a oD uvIARYOW uermoyeaeNn ueiuideyy b a uetumbex © a ueIOUOS wD a ueiqeqrey ueIsowlayy a uerquinjoyn & a a ueruersino'y uexay, uedynewey & o>) eo uewuooleg ioe) Lal uUBIURMIYO}eYASeS De tol sp) 4 a onl ton! taal i=} onl 3 é ka wb hy © 3 © 3 a 3} a LT 9T SGT uesuey uerlurporey) usrourll] uelueysel[V UBIIBIS te POG COLLET, ueIuoZ319, ueLIaAnooue A UEPeIOIOD co ueIUuR OW oo ueIpeuesy ‘A uvipeuesy ‘Wy uvluospny “y ueIuOspnyy “A ueruoyn, 0 uelnely ueysely ueounysa “MA UeOUWIYySY “| ueAesuyQ (‘panusjuon) ‘TT aATavy, 603 286 UvIUIpIeUIag URS WIC LAG re roo TE) UBIARYOW, uva}yeyW ues Be ri ueluoyeaen uviideyy uerluinbe x uvioUuos uviqeqrey ueISaula}IV uerquin[o7) ueIUeISInO'T uexay, uedr[neue 7, ueIuoo[eg UBIUBMIYO}VYSeS uesuey ueIUT[OIeD ueroury|y uviueysal[y UBIIAIS uenproquinyy (Continued. ) ueIuosI19 UkTIDANOOUL A uepeiojon TABLE 1. ueluejUOW LAVAS FOL HN uvIpeuey “y ueruospnyy ‘q ueluospny ‘A uemoyNn { uelnely ueysely UBOULIYSY “A uvoullysy “A ueAaesuy) 1 2E2W 3 4 5 6W6E 7TETW 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 SYSTEMATIC ZOOLOGY x x < re 9 ox x x x x x x X x xX 4 x > ey Ok x xX x x x x x > > Gey < KK XexK XX x x x xX & x x x xX x xX ax xxx x x MX x KK OX xX xx xX Kx xX x KO OX x x x xX X x xX x x x x OX x Xx x x Xx x x x x xX xX x &X x x x x x X x x xX &X x x X x xX &X >< 8 x X xx XK xX x x x x x x xX &X Xx > >< x x x x x xX xX & x x X Pk x x x x xX x PRN x x OX x x x x xX xX x x X x x x x x KX KX x x X x xX Xx < x x x x ~ x xX x x x xX x xX x x xX X x xX x X x x x xX xX x x xX xX x x >< x x x x x xX x xX x x x x x DRS Ieee x x xX x x x x x x X XS EX x x-xX x xX x x x x x x > aes x x x x x MK KX x x x x x x x xX x x OX Xx x x x xX eX x x x xX x X x x xX x x xx x x XX OX x x X x x x X x x x x x x ne Pas x X Xx x xX x x x x xX x xX x xX x x x xX x x x x xX 3 ie) g g s : 5 Se = Ze a = “ a5 3 = WS Sg 3 2%. SG See sa) wes S = REPEESE SES 2 SESETTESS EG RERSE GS BES SESS SES 2 S832 ee 2258455 S205 28 88 SESESSSSTESESASETS PSE LEE SS ESE RES 838 Seuss NESSES Sees ase sckdudsacdcseE ses 604 (Continued. ) TABLE l. DISTRIBUTION OF NORTH AMERICAN MAMMALS 287 UvIUIPIeuag US uerqeiqd ULTUIOF TED x x x x x uvIARyOoW uvoyeyy ues x x x ueQuiy x x x x x uvluoyearN ueIUideyy x xX x x xX x uevrumbe x uvi0uos x xX KX X KX XK X x x x xX KX XK EAC EZ LED f uvIsouloy x KX KX KX KX KX KX XK X x NED OS Se OS AES, 5 Oe 5 ueiquin[oy UBIURISINO'T x uexay, x x uevdr[neule fj, x xe eS Ke OX x X X uviUoo[eg MxM Me KKK KX KK XK x ee eS ON OG a eS a BS URIUBMIYI}EASES x XS Oe XX, o uvsuevy uBIUT[OIeD x uefoury |] x x xX Mx KOK XN KK K Oe KX XK x uviueyseal[V x MK KK XO KK KK KK XK KK XX uUviIaIS urnploquiny] KK OX uvluosI1Q, UBIIDANOIUE A uepeI0[O‘) x Sa PO aK uviue}UOsy x uurpEoE Mh uvipeur ‘y uvruospnyy “Y XK KX XK Ke KX XK XX xxx XO KK x xX xX xX uvtuospnyy * AA uvtuoyN DCG ee a OX uvynaly Nee BC a OOS OS Oe SS mes x DC a eS OX Ke aX x uvysely uBOUILysH “AA UvOUTYSY ‘of XK KX Ke KK x Se eX 1 2E2W 3 4 5 6BW6ETE7W 8 9 1011 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 x ee BG OC DOK ON 8K OS OG OS OSE ON uvAesuy) Conepatus leuconotus Lutra canadensis Felis onca F. yagouaroundi Lynx canadensis Mephitis mephitis L. rufus Mustela erminea Spilogale putorius M. macroura Martes americana M. rixosa Bassariscus astutus Procyon lotor Nasua narica M. pennanti M. frenata M. nigripes M. vison Gulo luscus Taxidea taxus F. concolor F. pardalis F. wiedii 605 x xX x XK x x x X KX KX KX KX XK XK X x x x xX x x x XxX KK KK K XK XK x KX KX KX XK x LG ee 2 OS x KX Kh eK x X X X KX KX KX KX KX XK X x x Cervus canadensis Dama hemionus D. virginiana Alces alces Rangifer tarandus Tayassu tajacou x «MX K KKK KX XK X x xX KX xX X x X KX KX KX KX XK XK X Antilocapra americana Bison bison Oreamnos americanus Ovibos moschatus Ovis canadensis O. dalli x X KX X KX K XK X 288 SYSTEMATIC ZOOLOGY Neo NW WG A\\ \ Sano oan oN SN VY WCCN foe \e 40| 27 |32 | 37 |43 & a 22|/5|23|33|32| 4846/62] a& zalzal zr [ov | srlse| ea] ee] 0? 76|/#| /8 |28|26 o fe] |7 [a [2 arlze lac oe rare aaah |v ola 70 | 9 | vo |ys'\/7 Jas|2/|2z [28 feet ven [ellis EAENEACIE 7174 AENEID Ie /¥\(0 | /3 2220/34) 3/|47 | 64) ¥5| 47/3532 | 37 U9 |s2\76laolas 23|28|39 33|36|3/ \z¢|25 /9| 60| 6 / ess YUU: HY BES 72S Bate eae SEEN TE cc om oe Ge oe WE PT Bed | eee, EERE eB aneaee A YY 250G so} WG] -]~ 31% RIS] s VISly SIRLa sale HEE BE wis [a gras SEE AR xfs aE ne LSE SECEEERELED N N Foe as ed es s }4[7 [7 [/4\72 8 |/s"|2/ |20 * ee fe pel [ale a lelea [ee 7 rae om [rr fae [vforlv ae [to [ala [lela mle | [ela forlacloolze or ales 14 [7s |/7 [27 |2¥| 40] 86] 27 [94] 37 [¥/ [23] 23/23] 34/47] 24/27 [22] /s'] + 3/6 30| // | /2| /2| 25 32 j2¥]/9|/s| 6 [3] EZ /1:\ 9 \23 | /6\/9|26\28)/6|\20\/9 30|32|36|24] 24|/3 | 33| 40 7 || # |ve|77| 7 | 77| 28 |20|/s'| 9 |8 |27| 24] 37] 33/25] 73 [24] 28] 54] 44 $ 23|/s'|/8|/7 35|28|47|¥0| 28 /2 [27| 3/| 45] #9) 4 N wy & N 4 & a N ~ i) NY ale|N | alr} oe w \ © Hl e}wo] RIN] & sag \ fe} = 5) w N & & ~ be ~~ [S| ty ~ Gq be. N re zt \ Gl @ * ‘ N LS gi “ N be ~ ~ 3 N a wisn BE raf a[s | 4 NH ]N A ns NE =F SIRS s[a 3] sls yh AS SAIS Piles e|& IE AR ole S|3 le AE Ps] a AA £13 no oH IS HB S| a5 epee lr fa [7 7 |7 [ae es eel omar om 7 [zo x94] # [ze] [09] |r [aoa [oe 7 7 [=| |2 [2323] 27 [| [20 ze [2624 20|27|-A| 20]30| 20s [27 [2olz0|2/[as90 >] =|-#lee]# [22 |e] ee 77373] a0] 2 [2s] 9 | [2 [as 222526] 2] 25 [20] 2a 27f07| 3 A fas] 7s [2324] # a] Vs [as |-4] 20 fee |zo] eelze]30] a] 29 ]ze|eelerfes|er| Soo Sas [ofofo DE 66 -/o0 43-65 Faye] ax- 42 [LT Je Se, Fic. 2. Final trellis or matrix giving Coefficients of Community (percentage of species common to pairs of provinces). Ordering of provinces is that resulting from cluster analysis. Heavy lines outline superprovinces and subregions. The classes of shading shown in the mirror image are determined by the critical mean CC values used to obtain higher categories of areas. 606 DISTRIBUTION OF NORTH AMERICAN MAMMALS 289 consisted of laying a transparent overlay over the species IFC map (H & S, Fig. 1) and drawing lines through all regions of high IFC value, delimiting ultimately a total of 86 (rather than the original 24) primary areas. The distribution of these is given as Figure 1. The genus IFC map was not used in the corrected analysis. Subsequent procedure was that of our earlier paper. Species checklists of each of the primary areas were prepared, and CCs were computed and subjected to cluster analysis. Because of the large number of CCs involved (86! = 3,741), calculation of CCs in this and subsequent operations was done by computer. In our earlier paper (H & S: 137-138), a mammal province was defined as an area with a mean CC of 62.4% or less, when com- pared to other areas by cluster analysis. This decision was based on the work of Preston (1962), who found that analysis of faunas by means of a “Resemblance Equa- tion” (RE) indicated that values of z (as derived from the RE) of about 0.27 repre- sented the break between faunistic homo- geneity and heterogeneity. In our earlier paper we converted z to S (Similarity), where S = 100 (1-—z), and calculated both S and CC for all items in the matrix. These were compared by regression, giving a slope b=1.17+ 0.02. Conversion of Preston’s critical z value to S gave an S of 73%, and conversion of the critical value of S to CC equaled 73/1.17 = 62.4%, and hence our use of this value. We did not, however, allow for the effects of statistical error. If this is incorporated, in the form of plus and minus two standard errors (providing limits at the 95% level of probability), the critical CC value falls within the range 60.30-64.60%. As a result, in this and subsequent papers I propose the use of a CC value of 65% as critical for the determination of mammal provinces. This is a conservative standard, and all values lying between 60 and 65% should be considered suspect, and are re- ported. The results of cluster analysis were evalu- ated according to this new standard. Pairs of primary areas with CCs higher than 65% (as determined by actual calculation or by averaging during cluster analysis) were pooled to create secondary areas. The whole process was then repeated. A new species checklist was prepared for each area, CCs were computed and _ subjected to cluster analysis, and a new dendrogram prepared. Pooling of areas was again done where CC values were higher than 65%, In all, four such sets of sequential opera- tions were carried out. In the final opera- tion, the total number of primary areas had been reduced from 86 to 38 secondary areas, all but three of which had CCs lower than 65% (2E and 2W, 6E and 6W, and 7E and 7W; see Figs. 2 and 3). These three sets of secondary areas were not pooled because they occur over large geographic areas and because I was concerned with their detailed analysis. The 35 secondary areas with CCs less than 65% constitute mammal provinces by the standards used here and are so treated, although two pairs of these fall within the questionable range 60-65% (15 and 16, 34 and 35, see Fig. 4). Figure 2 is the matrix resulting from cluster analysis, showing ordering of provinces and Coeffici- ents of Community between pairs. Figure 3 is a map showing geographic distribution of the provinces, and Figure 4 is a dendro- gram delineating the faunistic relationships existing between provinces, as determined by cluster analysis. A species checklist for each of the provinces, as it was used in the final operation, is given as Table 1. In our earlier paper (H & S), mammal provinces were grouped into the higher cat- egories of superprovinces, subregions, and regions. The method used in deriving these was to draw lines across the dendrograms at suitable CC levels, the choice of CC level being arbitrary but providing what ap- peared to be a useful classification (H & S: 139-140, 149). I have tried here to make as little change from the original scheme as possible; however, a small number of minor adjustments have been necessary. The 0-8% CC range of the dendrogram still stands as a level useful for the category 607 290 ALASKAN ALEUTIAN VANCOUVERIAN DIABLIAN CALIFORNIAN SIERRAN KANSAN SYSTEMATIC ZOOLOGY EASTERN HUDSONIAN .- eed \ 4 sa2aeaoam ? \ 7" rat EASTERN CANADIAN \ Soon VE A ILLINOIAN i | eared ; \ SIANIAN ! : - fj _toul ‘ Fic. 3. Final grouping of primary areas into mammal provinces. Broken lines indicate subdivisions of provinces. The approximate relationships of island faunas are also shown. of region. At this level, one region, the Nearctic is isolated. Subregions in our ear- lier paper stood between the 20-25% CC range; this is changed here to the 22-27% CC range, and still encompasses four subre- gions, following Wallace (1876). The cate- gory of superprovince was, in the earlier paper, set at a mean CC level of about 39%. The selection of this value was based on conclusions reached by Savage (1960), de- tails of which may be obtained from H & S, p. 1389-140. The 39% level would, in the case of the dendrogram used here (Fig. 4) give 11 superprovinces. Several cluster at a level very little higher than this, and I have arbitrarily moved the limit up to about 42.5%, so as to encompass these, giving a total of 13 superprovinces. These decisions > Fic. 4. Final dendrogram showing relationship between provinces. Ordering of provinces and mean Coefficients of Community (CC) are the results of cluster analysis. Solid vertical lines show mean CC levels at which regions, subregions, superprovinces, and provinces segregate. The three vertical lines for provinces represent the mean critical value plus and minus two standard errors. Per cent similarity is mean Coefficient of Community (CC). The “diamonds” of provinces 2, 6, and 7 represent the mean CCs at which the subdivisions of these provinces pool on cluster analysis. 608 DISTRIBUTION OF NORTH AMERICAN MAMMALS r~) -) zo Jo #o so [x-) To r [-) t Z-) 2 &@ yeaa tt BD PSS B= 2 Ee ee Ee Be Oe ee Ee ee es eee eS Ub cand pale ol a ee ee ee ee svua- REGIONS SUPER- Reston? PROVINCES PROVINCES 609 100 <= % Semilari UNGAVAN ESKIMOAN ALASKAN ALEUTIAN YUKONIAN HUDSONIAN CANAD/AN MONTANIAN COLORA DAN VANCOUVERIAN OREGONIAN HUMBOLDT IAN S/ERRAN ALLEGHENIAN 4LLINOIAN CAROLINIAN KANSAN SASKATCHEWDANIAN BALCONIAN TAMAULIPAN TEXAN LOU/S/ANIAN COLUMBIAN ARTE MESIAN XAIBABIAN SONORAN YAQUINIAN PIAPIMIAN NAVAHON/AN UINTIAN SAN MATEAN MOMAV/AN CALIFORNIAN DIABLIAN SAN BERNARDINIAN y 291 292 SYSTEMATIC ZOOLOGY continue to fill the desirable requirements outlined in our earlier paper. Good single values for each of these hier- archic levels would be: provinces 62.5%, superprovinces 42.5%, subregions 25%, and regions 5%. By this scheme the 35 mammal provinces of North America are grouped into 13 superprovinces, four subregions, and one region. These are named and their dis- tributions mapped on Figures 5a and 5b. They are also blocked out in the matrix (Fig. 2) and marked by lines drawn at ap- propriate CC levels on the dendrogram (Fig. 4). The problem of nomenclature of mammal areas is discussed subsequently. The nearest approach to the biotic prov- inces of Dice (1943), and Kendeigh (1961 ) through the analysis carried out here, is ob- tained by fitting a line at about the 54% CC level of the dendrogram. The more in- tuitive decisions of these workers implies a degree of segregation about 10% lower than the one used here. Nomenclature and Status of Areas No changes in the names or status of regions or subregions over those of our earlier paper have resulted from the reanal- ysis. Because of the increase in numbers of provinces however, minor adjustments in these and in other categories have been obligatory. As few name changes as possible have been made. Where new names have been applied, an attempt has been made to take them from the literature and to apply them on the basis of priority. Where there has been need to coin names, I have tried to follow the spirit of earlier workers. As an aid to recognition, names of provinces are in the form of adjectives, names of super- provinces in the form of nouns. Those cases in which provinces segregate within the doubtful 60-65% CC range, or in which segregation occurs at a level only slightly higher than 65%, are here de- scribed. More detailed analyses will doubt- less result in some changes in status within these groups. The following provinces are new and have been named by me: no. 1, Ungavan; no. 12, Humboldtian; no. 25, Kaibabian; no. 30, Uintian; no. 31, San Matean; no. 34, Diablian and no. 35, San Bernardinian. Those provinces that are new but that have been given an older name are, together with the source of the name: no. 3, Alaskan (Allen, 1892); no. 5, Yukonian (Cooper, 1859); no. 10, Vancouverian (Van Dyke, 1939); no. 13, Sierran and no. 23, Colum- bian (Miller, 1951). The names Saskatche- wan and Mapimi are here converted to the adjectival forms, Saskatchewanian, and Mapimian. The Hudsonian (no. 6) is a new province. The name was formerly applied to the prov- ince here termed Canadian (no. 7), and the Canadian of earlier workers is here termed Alleghenian (no. 14), following the precedence set by Cooper (1859), and Allen (1892), after Kendeigh (1954). The Carolinian (16) is a new province. The name was applied to what is here largely represented by the Louisianian province (22), in our earlier paper. Its present ap- plication is the correct one, however, by the standards of older workers. The Louisian- ian should properly be called the Austrori- parian, following Dice (1943), Kendeigh (1961), and H & S. Because it has super- province as well as province status, and re- quires the nounal form of the same as well as an adjectival one, I have applied Allen’s (1892) terminology to it. Not all provinces segregate clearly. The northern limit of no. 3, the Alaskan, was dif- ficult to locate, it being a region of broad transition. Its mapped limit is relatively arbitrary. The Sitkan province of H & S is here included in the Yukonian (no. 5), and the Vancouverian (no. 10), clustering with the former with a CC of 76%. That part of the Yukonian province made up of the Brooks Range very nearly segregates with a CC of 66%. The Eskimoan, Hudsonian, and Canadian provinces (nos. 2, 6, and 7) have, for rea- sons given elsewhere, each been split into eastern and western components. Of these, 610 DISTRIBUTION OF NORTH AMERICAN MAMMALS 293 a. SUBREGIONS NAVAHO b. SUPERPROVINCES Fic. 5, a and b._ The distribution of mammal subregions and mammal superprovinces, as determined from the dendrogram. the Eskimoan components cluster with a CC of 67%, and the Canadian with a CC of 66%. These are nearly critical values, indi- cating that the components almost merit province status. The Oregonian (no. 11) almost segre- gates into western coastal and eastern Cas- cadian provinces, pooling with a CC of 66%. The Alleghenian (no. 14) segregates from the eastern component of the Canadian (no. 7) with a CC of only 64%, a critical value. It clusters with the Carolina superprovince on analysis, however, and does so with prov- ince rating. The Carolinian (no. 16) is not a clearly defined province and probably should have been pooled with the Illinoian (no. 15), the two clustering with a CC of 64%. The Car- olinian is made up of three distinctive geo- graphic components; that east of the Appa- lachian Mountains clusters with the rest of the province with a CC of 67%, and that of the Ozark Mountains clusters at 66%. Two of these components are distinct enough from the Ilinoian that I have provisionally kept the Carolinian as a full province. The Balconian (no. 19) was incorrectly identified by H & S as part of what is here called the Tamaulipan (no. 20). The Bal- conian in its present sense stands as a full province. The Louisianian (no. 22), under the name Austroriparian, was in part identified as the Carolinian by H & S. Its distribution as determined by reanalysis is the more realistic one. The larger part of the Columbian prov- ince (no. 23) was named Artemesian by H &S. The latter term is here applied to a restricted portion of the Columbian as prov- ince no. 24. The Palusian of H & S is here pooled with the Columbian, with a CC of 70%. The Mohavian province (no. 32) presents something of a puzzle. It was not recog- nized through examination of the IFC map but appeared through scrutiny of individ- ual species maps. Once recognized, how- ever, cluster analysis caused it to segregate out to the extent of meriting superprovince status, and I have accepted it as this. Its geographic limits, however, have been de- 611 294 SYSTEMATIC ZOOLOGY termined subjectively, and they should be considered as suspect. The Diablian (no. 34) is also of uncer- tain status, as it clusters with the San Ber- nardinian (no. 35) with a CC of 61%, a critical value. Because not all of the latter occurs in the area studied, its analysis is incomplete, and for this reason the distinc- tion is provisionally accepted here. Of superprovinces, the Texas, Columbia, Mapimi, and Mohave are new, and the names Hudson and Austroriparian of H & S are replaced by the names Canada and Louisiana, for reasons given elsewhere. Insular Faunas Sixty-four species (27%) of the total mammal fauna occur on the larger islands adjacent to the continent and on the islands of the Great Lakes. Insular faunas were in each case compared with the faunas of several of the nearest mainland provinces by means of the Coefficient of Community and Simpson’s Coefficient (SC). The latter is a measure of the percentage of species occurring on an island that also occur in in the mainland province (Simpson, 1943; H &S: 131). Results are given in Table 2. Most island faunas give a CC much lower than Preston’s critical 65% value when com- pared with the faunas of adjacent mainland provinces (Table 2). Most islands would therefore merit full province status, if this standard were to be applied. The generally low CC obtained, however, is the result of the small size of insular faunas, a bias being introduced as a consequence of it. Simp- son’s Coefficient is, in these circumstances, a more reliable measure, and I attribute greater significance to it. No critical value of SC is available, however. Because of this, and because there is more interest in similarities than dissimilarities, island faunas have in all cases been named as part of the fauna of the adjacent province to which they show nearest relationship as determined primarily by Simpson’s Coef- ficient. TABLE 2. No. of Adjacent Island species provinces cc sc Long Island 29 14 Alleghanian 51 93 16 Carolinian 52. «61 14 Alleghanian 55 94 7E E.Canadian 64 87 7E E.Canadian 68 93 Cape Breton 31 Prince Edward 29 Island 14 Alleghanian 48 90 Anticosti 5 6E E.Hudsonian 17 100 7E E.Canadian 13 100 14 Alleghanian 10 100 Newfoundland 12 6EE.Hudsonian 40 100 7E E. Canadian 28 92 14 Alleghanian 19 83 Belcher 3 1 Ungavan 25 100 6E E. Hudsonian 10 100 7E E. Canadian S33 Manitoulin 25 14 Alleghanian 49 100 7E E.Canadian 62 96 Isle Royale 9 7EE.Canadian 24 100 14 Alleghanian 18 100 Arctic Archi- 10 2EE.Eskimoan 67 100 pelago 1 Ungavan 57 ~=80 Kodiak 12 5 Yukonian 33 100 4 Aleutian 57 92 3 Alaskan 39 85 Alexander Archi- 21 10 Vancouverian 61 95 pelago 5 Yukonian 44 90 Queen Charlottes 12 10 Vancouverian 36 92 5 Yukonian 24 83 Vancouver 22 +11 Oregonian 33-83 10 Vancouverian 54 #79 Long Island shows closest relationship to the Alleghenian province (no. 14), not the Carolinian (no. 16), as might have been expected. Cape Breton is nearest to the Alleghenian by Simpson’s Coefficient; I have placed it there though it shows a very high CC with the eastern Canadian (64%). Prince Edward Island lies nearest to the eastern Canadian province (no. 7E), which is surprising in the light of its geographic proximity to the Alleghenian. Anticosti is grouped with the eastern Hudsonian (no. 6E ), on the basis of its high CC, as is New- foundland, the latter on the basis of both coefficients. Belcher Island is, because of its CC only, treated as being most closely related to the Ungavan (no. 1). Manitoulin has highest SC with the Alleghenian, high- 612 DISTRIBUTION OF NORTH AMERICAN MAMMALS 295 est CC with the eastern Canadian, but be- cause greater weight is given to Simpson’s Coefficient, I have grouped it with the Alleghenian. Isle Royale shows closest af- finity with the eastern Canadian province. Of the islands of the west coast, the Alex- ander Archipelago and the Queen Charlotte Islands show closest relationship to the Vancouvarian (no. 10). Vancouver Island, on the basis of its SC only, is closest to the Oregonian (no. 11). Kodiak Island has highest CC with the Aleutian (no. 4), but highest SC with the Yukonian (no. 5), and following the policy set previously is considered most closely re- lated to the latter. Of the Arctic archipelago and Greenland, the following groups of islands have identi- cal faunas: group 1, Baffin, Southampton, and Coats islands; group 2, Somerset Island; group 3, Banks Island; group 4, Greenland, Sverdrup Islands, Borden and Prince Pat- rick islands; group 5, Victoria, Prince of Wales, Melville, Bathurst, Cornwallis, Devon, and Ellesmere islands. The faunas of these groups of islands, together with those of the Ungavan and eastern Eskimoan provinces (nos. 1 and 2E) were analyzed by first computing Coefficients of Com- munity between them, then subjecting these to cluster analysis, using the methods outlined previously. All of the island groups cluster at a mean level of 61% or higher, falling within the critical range or better. The groups taken together segregate from the eastern Eskimoan with a mean CC of 54% and from the Ungavan with a mean CC of 44%. The equivalent mean SCs are 100% and 85% respectively. As a result I have treated all of the Arctic archipelago and Greenland as part of the eastern com- ponent of the Eskimoan province. A generalized mapping of these relation- ships is given in Figure 3. It should be noted that the affinities of Cape Breton, Prince Edward and Long islands are indi- cated incorrectly here. Discussion The general conclusions reached as a result of this re-evaluation differ in no way from those obtained through our earlier analysis (H & S; 147-151), and they are not treated further. It is important that the subjectivity of the methods used here be kept in mind however. The sources and attempted controls of these have been dis- cussed in our earlier paper (H & S: 148- 149, 151) and include taxonomic errors, dis- tributional errors, choice of point or block for sample; size of sample block, fitting of isarithms, selection of primary areas, choice of coefficient of association, choice of clus- tering method, and others. The methods used here are ideally suited to computer techniques. This reanalysis could not in fact have been completed within reasonable time had such techniques not been available. Miller, Parsons, and Kofsky (1960) have described the use of so-called successive scanning mode micro- densitometers, which automatically map the densities of films and other kinds of trans- parencies. Such devices are sold by Beck- man and Whitley of San Carlos, California, under the registered trade name of Iso- densitracer. The use of such a device on a transparent map showing the distribution of all North American mammals drawn in inks or paints which gave progressively less translucency as additional layers were added, would be ideal in the development of more refined IFC maps. The IFC map used in this work (H & S, Fig. 1) was based on the computation of the percentage of species whose ranges ended within blocks 50 miles to a side. The abso- lute value of an IFC is a function of size of block (H & S: 148). I suggest that any future use of IFCs incorporate as subscript to values given, a statement of the area of the block in kilometers. Converting size of block used here to square kilometers gives an area per block of approximately 6,500 square kilometers, and the IFCs used here are symbolized as IFC¢,500. Subscripts made up of a statement of length of side of a block rather than area would be less cum- bersome. I suspect however that circles 613 296 may prove more useful than blocks as sam- pling units, especially if microdensitometers are used, which make the use of area necessary. Since preparation of our earlier study, a number of similar papers have been drawn to my attention or have been published. Munroe (1956) gave a fine account of the ecologic and zoogeographic features of Can- ada and an analysis of the insect faunas of the continent. Udvardy (1963) provided an excellent analysis of the bird faunas of North America. His methods differed from ours in that, rather than treating all species simultaneously, he grouped them by type of distribution pattern, and then prepared maps showing numbers of species geo- graphically, by type of pattern. By this method he was able to recognize the pres- ence of 17 primary faunas and 25 secondary ones. The methods used, while different in basic respects from those used here, could easily prove to be more useful. The following should be added to our earlier summary of coefficients of associa- tion (H & S: 131-132). Smith (1960) used the term “Faunistic Relation Factor” (FRF) for the Coefficient of Community, and Huheey (1965) called it a “Divergence Fac- tor’ (D), when subtracted from 100. Fager (1965) has devised a new coefficient in the form of 100 C/\/nyne-%\/no, where nj is less than ng. Long (1963) gives a review of coefficients and suggests use of an “average resemblance formula” first used by Kulczn- ski in 1927, and listed in H & S, p. 1982. In our earlier study (H & S: 128-129, 148) we pointed out that our work has been based on Webb’s (1950) analysis of the mammals and herpetofauna of Texas and Oklahoma. The work of Ryan (1963) who improved on Webb’s technique in analyz- ing the mammal faunas of Central America was not known to us at the time. Subse- quently, Huheey (1965) published an ac- count of further modifications of the tech- nique in the study of the herpetofauna of Illinois. Since the methods used in all of these are related, and because they are sim- ilar in principle, their comparison may be of SYSTEMATIC ZOOLOGY interest, and I have attempted to do this briefly in the account following. Webb’s (1950) method was to lay a grid of sample points at 100-mile intervals on a map of the area to be studied, to prepare a species checklist for each sample point, to compute Coefficients of Community between sample points and then plot these, to draw lines connecting CCs of equal value, providing a form of “contour map,” and to consider “valleys” with CCs of 75% or more as “bio- geographic regions.” A key point underly- ing Webb’s analysis lies in the fact that he found CCs computed in a north-south plane to differ statistically from those com- puted in an east-west plane. Since he found that the east-west data gave most significant results, he accepted these in the preparation of his final map and rejected the north-south data. Webb deserves com- mendation for being first, to my knowledge, to devise a numerical technique for biogeo- graphic analyses in two dimensions. Ryan’s (1963) analysis used a methodol- ogy only slightly different from that of Webb. Because of the unusual shape of the area studied, the grid of one portion of it was made up of points 100 kilometers (about 62 miles) to a side, of a second por- tion of it, 50 kilometers (about 31 miles) to a side. CCs, called “Similarity Values” by both Webb and Ryan, were calculated for both the north-south and east-west planes, and both sets of data were used in prepara- tion of the final contour maps, so far as I can determine. Ryan called the contour lines “isobiots.” It is not clear whether Webb’s 75% rule for biogeographic regions was used. Huheey’s (1965) method differed to some degree from the preceding. It was to lay a grid of 20 miles to a side onto the area to be studied. Within each block of the grid a species checklist was prepared. For each of the four sides of all blocks, a Divergence Factor (D) was computed, where D= 100-CC; thus D is the complement of the Coefficient of Community. Huheey refers to the CC by Smith’s (1960) term, “Faunis- tic Relation Factor,” or FRF. The average 614 DISTRIBUTION OF NORTH AMERICAN MAMMALS 297 of the four Ds for each block was computed, this being the mean D for that block. Fin- ally, contour lines called “isometabases” were drawn around mean Ds of equal value. From the contour map herpetofaunal re- gions were described. Webb’s and Ryan’s methods, it will be observed, are essentially the same, differing only in distance between sample points and planes in which CCs are computed. Hu- heey’s method, and the method used in this and in our earlier study differ considerably, though they seek identical ends through development of contour maps depicting faunistic change. I have been led to under- stand that still other techniques and refine- ments of those discussed here are in prepa- ration. For example, Valentine (1965) re- ported a study of the distribution of north- eastern Pacific molluscan distributions us- ing methods similar to those employed in this and in our earlier paper. It is apparent that there is need for a comparative testing of the several methods of analysis presently at hand, using the same basic materials in each. I plan to attempt such a study. Earlier (H & S: 129), we mentioned a partial testing of Webb’s original method on the mammal fauna of North America. In view of the preceding, a brief account of the testing follows: Webb’s method was followed exactly, except that the grid of sample points was placed on a northeast- southwest plane, giving better coverage of certain coastal areas. A number of varia- tions in the planes in which CCs were com- puted were attempted. These variations included: (1) computing and plotting CCs in the northeast-southwest plane only; (2) doing the same in the northwest-southeast plane only; (3) averaging adjacent CCs taken in both planes and plotting these; (4) plotting highest CCs only of pairs computed in both planes. We did not try Ryan’s device of plotting all CCs taken in both planes. However, of the variants tested, none gave results that appeared anywhere near reasonable in terms of what we knew generally of the distribution of biogeo- graphic and ecologic zones. The variants used by Ryan and Huheey, however, ap- pear to work well on the basis of their evidence, and my conclusions apply in no way to their results. No attempt has been made to take into account the effects of altitude on mammal distributions. Dice, in his original study of biotic provinces (1943) described such ef- fects in terms of “life belts” and named a number of these. Kendeigh (1954) on the other hand did not see altitude as a con- founding factor in delimitation of biotic provinces. He wrote: “A mountain range may have several life zones represented on it, but only a single biotic province, pro- vided there is a similar tendency for specific or subspecific distinctiveness of the fauna in all the zones. The two concepts there- fore have quite different objectives.” I have not been able to decide which of the two views applies in studies of the sort carried out here. It should be realized, how- ever, that the methods employed here are capable of analyzing the effects of altitude on distribution, and segregating altitudinal provinces, if they exist, given distribution maps of sufficient accuracy in the first place. The maps used here failed to show details of vertical distribution, and as a consequence this aspect of the problem has not proven solvable. An attempt was made to analyze altitud- inal distribution in a different way. Each species of mammal was given its life zone distribution, this information being collated from a large number of sources, chiefly certain of the North American Fauna Series. The faunas of each of the life zones within provinces occurring in generally mountain- ous parts of the continent were treated as primary areas, Coefficients of Community were computed, and the results subjected to cluster analysis. The initial results were un- satisfactory, however, and because of this and because of the circularity of reasoning involved, the method was abandoned. No attempt has been made to relate the distribution of mammal areas to the distri- bution of other natural units, either physio- graphic, climatic, or vegetational, although 615 298 a comparison of Figure 3 to maps showing the distribution of such features (e.g., Lobeck, 1948; Thornethwaite, 1948; Rowe, 1959; Shantz and Zon, 1923), shows that the relationship is very close. Summary 1. An earlier study demonstrated that range limits of North American terrestrial mammals were grouped, and that regions of faunistic homogeneity could as a conse- quence be identified. 2. The method used to identify such regions was to compute percentage of spe- cies whose ranges ended in blocks fifty miles on a side (IFCs), and to then fit isarithms. Topographic “valleys” in the map represented regions of faunistic homoge- neity, or “primary areas,” and for 24 of these, species checklists were prepared. The percentage of species common to pairs of primary areas (CCs) were computed, and the results subjected to cluster analysis, us- ing the method of weighted pair-groups with simple averages. This resulted in a matrix and dendrogram showing relation- ships and ordering of primary areas. Using a conversion of Preston’s Resemblance Equation, a CC of 62.5% was considered critical. Primary areas with a CC lower than this were considered “mammal provinces.” By this criterion, 22 mammal provinces grouped into nine superprovinces, four sub- regions, and one region were recognized. 3. Many more primary areas should have been derived from the IFC map. Starting with 86 primary areas and carrying out four sequential sets of cluster analyses leads to the conclusion that a minimum of from 33 to 35 mammal provinces occur in the con- tinent. These are mapped, named, and briefly described. For statistical reasons, the upper limit of Preston’s critical value is raised to a CC of 65%. 4. Higher categories of mammal areas are derived by grouping the provinces on the matrix and dendrogram at appropriate mean CC levels. A mean CC of 42.5% gives 13 superprovinces; a mean CC of 25%, four SYSTEMATIC ZOOLOGY subregions; a mean CC of 5%, one region (the Nearctic). These are mapped, named, and briefly described. In general, provinces are named as adjectives derived from geo- graphic place-names, superprovinces as nouns. Where possible the names of these and of regions and subregions are taken from the literature on a priority basis. 5. Approximately one-quarter of the mammal species of the continent also occur on nearby continental islands. Island faunas are always smaller than those of the adja- cent mainland and always show closest faunistic similarity to nearby provinces. 6. The methods used have the advantage of being relatively objective, repeatable, and well-suited to computer operations. The use of a successive scanning mode micro- densitometer may prove useful in the prepa- ration of accurate IFC maps. 7. Accounts of several techniques in bio- geographic analysis similar in aim and method to those used here have recently appeared. These are briefly compared. There is need for a critical testing and evaluation of these to determine which provides the best basis for further refine- ment. 8. While the methods used here are suit- able for analyzing the effects of altitudinal zonation on distribution, lack of requisite detail in the distribution maps now avail- able makes such analyses impractical. 9. There appears to be a high degree of correlation between the distribution of mammal areas and other kinds of natural areas. REFERENCES ALLEN, J- AW 1892: tion of North American mammals. Mus. Nat. Hist. 4:199-243. Cooper, J. G. 1859. On the distribution of the forests and trees of North America .... An- nual Report Board of Regents, Smithsonian Inst.: 246-280. Dice, L. R. 1943. The biotic provinces of North America. Univ. Michigan Press, Ann Arbor. Facer, E. W. 1963. Communities of Organisms. In Hill, M. N., The sea, vol. 2, p. 415-437. HacmMeter, E. M., and C. D. Stunts. 1964. A The geographical distribu- Bull. Amer. 616 DISTRIBUTION OF NORTH AMERICAN MAMMALS 299 numerical analysis of the distributional patterns of North American mammals. Systematic Zool. 13:125-155. Huneey, J. E. 1965. A mathematical method of analyzing biogeographical data. 1. Herpeto- fauna of Illinois. Amer. Midl. Nat. 73:490-500. Jaccarpb, D. 1902. Gezetze der Pflanzenverthei- lung in der Alpinen Region. Flora 90:349-377. KENDEIGH, S.C. 1954. History and evaluation of various concepts of plant and animal communi- ties in North America. Ecology 35:152-171. 1961. Animal ecology. Prentice-Hall, Engle- wood Cliffs. Kuxczynski, S. 1937. Die pflanzenassoziationen der Pieninen. Bull. Internat. Acad. Polish Sci. Lett...1927 (2):57-203. Lopeck, A. K. 1948. Physiographic provinces of North America. Geographical Press, New York. Lonc, C. A. 1963. Mathematical formulas ex- pressing faunal resemblance. Trans. Kansas Acad. Sci. 66:138-140. Miuter, A. H. 1951. An analysis of the distribu- tion of the birds of California. Univ. Calif. Publ. Zool. 50:531-644. MILLER, C. S., F. G. Parsons, I. L. Korsxky. 1964. Simplified two-dimensional microdensitometry. Nature 202:1196—1200. Munrog, E. 1956. Canada as an environment for insect life. Canadian Entomologist 88:372— 476. Preston, R. W. 1962. The canonical distribu- tion of commonness and rarity. Ecology 43:185- 215, 410-432. Rowe, J. S. Forest regions of Canada. Bull. Ca- nadian Dept. Northern Affairs and Natural Re- sources 123, p. 1-71. Ryan, R. M. 1963. The biotic provinces of Cen- tral America as indicated by mammalian distri- bution. Acta Zoologica Mexicana 6:1-55. SavacE, J. M. 1960. Evolution of a peninsular herpetofauna. Systematic Zool. 9:184-212. SHantz, H. L., and R. Zon. 1924. Atlas of American agriculture. Pt. 1, Sect. E, Natural Vegetation. U.S.D.A., Bureau Agric. Economics, p. 1-29. Smpson, G. G. 1943. Mammals and the nature of continents. Amer. J. Sci. 241:1-31. 1964. Species density of North American Re- cent mammals. Systematic Zool. 13:57-73. SmitH, H. M. 1960. An evaluation of the biotic province concept. Systematic Zool. 9:41-44. SoxaL, R. R., and P. H. E. Sneatu. 1963. Principles of numerical taxonomy. Freeman, San Francisco. THORNETHWAITE, C. W. 1948. An approach to a rational classification of climate. Geogr. Rev. 38:55--94, Upvarpy, M. D. F. 1963. Bird faunas of North America. Proc. 13th Internat. Ornithol. Con- gress: 1147-1167. VALENTINE, J. 1965. Numerical analysis of north-eastern Pacific molluscan distributions. Paper read to the Pacific Division of A.A.A.S., Riverside, California, June 24. VaN Dyke, E. C. 1939. The origin and distribu- tion of the coleopterous insect fauna of North America. Proc. 6th Pacific Science Congress, 4:255—268. Wa.tace, A. R. 1876. The geographical distri- bution of animals. 2 vols. Macmillan, London. Wess, W. L. 1950. Biogeographic regions of Texas and Oklahoma. Ecology 31:426-433. EDWIN M. HAGMEIER is a member of the Department of Biology at the University of Vic- toria, Victoria, B. C., Canada. The work was sup- ported by the University and by the National Research Council. Mr. Peter Darling of the Uni- versity Computer Center has played an important part in the analyses reported here. The illustrations were prepared by Miss Elizabeth Swemle. The writer extends his thanks to both, and dedicates the study to S.E.H. 617 ANALYTICAL ZOOGEOGRAPHY OF NORTH AMERICAN MAMMALS? Joun W. Witsoy, III Department of Biology, George Mason University, Fairfax, Va. 22030 Received January 22, 1973 Latitudinal gradients in species diversity represent, perhaps, one of the longest rec- ognized and most discussed biogeograph- ical phenomena. Simpson (1964) studied the species density pattern of the mam- mals of North America and found a trend toward increased species density in the tropics; Terent’ev (1963) found similar results in the U.S.S.R. Simpson points out that the increase does not occur in all of the mammals, but in certain groups. The purpose of this paper is to begin the analysis of different mammalian taxa, and to show the significance of topographic re- lief and climate on which Simpson did not calculate statistics. METHODS The material for this paper conforms as much as possible to that used by Simpson (1964). A grid of quadrats 150 miles square (22,500 square miles) centered at 40°N, 100°W was imposed on a map of Lambert’s azimuthal equal-area projection (Goode’s series by Henry M. Leppard, ed., The University of Chicago Press) of North America to the Panama-Colombia border. Species lists were generated for each quadrat using the species distribution maps in Hall and Kelson (1959) for mainland species. Whenever Hall and Kelson sus- pected two species were only subspecies of the same species, I recorded them as one species. In all, species lists were made for 445 quadrats with a total of 671 species of mammals, which were the basis for all analyses. A copy of these species lists is included in Wilson (1972). * Portions of this paper were presented at meet- ing of the Society of Vertebrate Paleontology, 1970; and the Society for the Study of Evo- lution, 1971. EVOLUTION 28:124-140. March 1974 The topographic relief (difference in elevation of highest and lowest points within quadrats) in quadrats was deter- mined to the nearest 100 feet (30.5 m) using relief maps in The World Book At- las. Values of the estimated actual evapo- transpiration (AE), which is the actual amount of water evaporated from the ground or transpired by plants per year, and which are highly correlated with net annual above ground productivity (Rosen- zweig, 1968), were determined from a con- tour map made by Rosenzweig (pers. comm.), drawn with values of AE calcu- lated from data published by Thorn- thwaite Associates (1964). Both mean AE and range of AE per quadrat were deter- mined for each quadrat. To determine the effects of topographic relief and AE on species density of mam- mals in the temperate region, I used the quadrats between 40° and 50°N, where there is little latitudinal effect on species density, and compared species density in regions of high (5000 feet or more) and low (1000 feet or less) topographic relief and high (600 mm/yr. or more) and low 400 mm/yr. or less) AE. Coastal quad- rats which were less than half land were not used. The distribution of species among higher taxa in faunas, using the Shannon-Weaver information measure, was termed taxo- nomic hierarchical diversity (THDM). It was designed to be analogous to the hier- archical partitioning of species diversity proposed by Pielou (1967) and is derived in Wilson (1972). The equation used for calculating the measure was: oO Si THDM =HD,+ EP rs i 618 ZOOGEOGRAPHY OF NORTH AMERICAN MAMMALS ° ts Sy +E Yuba =e eS where 94; A Deg = - ») elie loge aie are Sij where o is the number of orders, F,z is the number of families in the 7th order, G,7j is the number of genera in the jth families of the 7th order, S is the number of species in the fauna, S; the number of species in the 7th order, S;; the number of species in the jth family of the 7th order, HDo is the diversity of species divided among orders, HD,» is the diversity of species divided among genera. Such a measure of taxo- nomic hierarchical diversity will have two components: the number of higher taxa and the equitability of the distribution of species among those higher taxa. The choice of 150 mile square quadrats used by Simpson (1964) is somewhat ar- bitrary. Large quadrats on the order of 500 miles would probably be inadequate to resolve important zoogeographic changes. On the lower end of the scale the distri- butional data on the whole are certainly not accurate within 10 miles. Murray (1968), while criticizing conclusions of studies based on data gathered by super- imposing quadrats on Hall and Kelson’s range maps, points out that Simpson avoids many problems with the basic data by his choice of a relatively large quadrat. Also, supplementary data such as AE are not accurate to much less than 50 miles. There are limitations with all range maps which draw a smooth line around all peripheral records and indicate the con- tained area to be a continuous distribution of the species. Species never occur over all of the included range; however they probably are not absent from anything approaching 22,500 square miles. There must be many errors in the distribution maps of individual species. However, it is not likely that there is any systematic bias 125 of more errors in any one region than others (Simpson, 1964) since the same people reviewed all species. This is a very important point; since there must be errors, a lack of systematic bias makes it likely that the trends I find will not be changed by the constant revision and improvement in our knowledge of the ranges and sys- tematics of individual species of mammals. Unfortunately this lack of systematic bias between areas of taxonomic groups is prob- ably not true in the data for any other part of the world, because no person has reviewed all of the mammals of another entire continent, except Australia, and the mammal faunas are not as completely known in the rest of the world. Hall and Kelson also attempt to produce maps which reflect reasonably natural conditions before gross environmental changes by man have changed drastically many species distributions, especially of larger mammals. This method overestimates sympatry in quadrats in three ways. (1) When dis- tribution maps overlap, species may never contact each other because of habitat dif- ferences. (2) Distribution maps are drawn to include all marginal records of the spe- cies. It is doubtful that a species ever in- habits all marginal points at the same time, or in fact, that many marginal points can be considered as places where the species is reproductively successful in even the short term; the presence of the species in these areas may be dependent on continued immigration. (3) The species was included in the species list of a quadrat if its dis- tribution included any part of the quadrat. This will overestimate sympatry most in topographically complex areas. This study considers only the number of species, genera, families, or orders in the quadrats; it does not take into account relative abundance of individuals or tro- phic complexity. Such studies would be quite informative, but censuses of mam- mals which contain no bias in counts of individuals for different taxonomic groups are difficult to compile and do not exist in the literature. 619 126 170 150 o ALL MAMMALS rs) Ww Qa ” 100 ww ro) a WwW S50 = z 0 80 N LATITUDE Fic. 1. Relationship of the number of species of all mammals in each quadrat and degrees north latitude shown with best fit polynomial regres- sion line (up to the fifth degree) to indicate the central tendency of the plot. Latitudinal Effects The general latitudinal increase in spe- cies density of the mammals was reported by Simpson (1964) and may be seen in a scatter plot of species against latitude (Fig. 1) and a contour map (Fig. 4). However the increase of species density into the tropics from the temperate regions is due primarily to the order Chiroptera, 170 ISO QUADRUPEDAL MAMMALS 100 50 NUMBER OF SPECIES N LATITUDE Fic. 2. Relationship of the number of species of quadrupedal mammals (all mammals except the Chiroptera) in each quadrat and degrees north latitude shown with best fit polynomial regression line. J. W. WILSON CHIROPTERA NUMBER OF SPECIES N LATITUDE Fic. 3. Relationship of the number of species of Chiroptera in each quadrat and degree north latitude shown with best fit polynomial regres- sion line. as can be seen in scatter plots of the quadrupedal mammals (the total mammal fauna with the Chiroptera removed) (Fig. 2) and the bats (Fig. 3) as well as in con- tour maps (Fig. 5, 6). In the graph (Fig. 2) and the contour map (Fig. 5) of qua- drupedal mammals, the regions of highest species density in the tropics and tem- perate region have approximately equal values. Both of these regions have high topographic relief. The bats, unlike the quadrupedal mammals, show a marked lat- itudinal increase in species density. While there is no increase in the species density of quadrupedal mammals from the temperate zone to tropics, there is some increase in the genus density (Fig. 7, 8), which is primarily due to the orders Mar- supalia, Edentata, and Primates. With the exception of the genus Marmosa (Mar- supalia) all of the genera of these orders are monotypic in the region studied. In the orders of quadrupedal mammals char- acteristic of the temperate region (Insec- tivora, Lagomorpha, Rodentia, Carnivora, Artiodactyla) there is a decline in genus density from temperate to tropical regions (Fig. 9). The pattern of species-per-genus of all mammals and quadrupedal mammals against latitude are essentially the same 620 ZOOGEOGRAPHY OF NORTH AMERICAN MAMMALS 127 MILES nuit DOWNSLOPE AAAA FRONT ALL MAMMALS Fic. 4. Contour map of the number of species of all mammals in each quadrat, 150 miles square. The contour interval between isograms is 5 species in the part of the map north of the approximate position of the Mexico-United States border south of that the interval is 10. The “fronts” are lines of exceptionally rapid change that are multiples of the contour interval for the region. Indication of the downslope side of a contour is given in the areas where this is not obvious at first sight. 621 128 J. W. WILSON MILES oui DOWNSLOPE AAA A FRONT QUADRUPEDAL MAMMALS Fic. 5. Contour map of the number of species of quadrupedal mammals (all mammals except the Chiroptera) in each quadrat. The contour interval between isograms is 5 species north of the south- ern edge of the Mexican Plateau and 10 south of there. 622 ZOOGEOGRAPHY OF NORTH AMERICAN MAMMALS 129 \ fe) NS \ \ nN \ Y \ \ ' ; CJ / 10 10 N \ 15 \ | | | I 20 15 / / / x S Ga Fic. 10. Relationship of the ratio of species per genus of (a) all mammals and (b) quadru- pedal mammals in each quadrat and degrees north latitude shown with the best fit polynomial re- gression line. J. W. WILSON TEMPERATE ORDERS NUMBER OF GENERA N LATITUDE Fic. 9. Relationship of the number of genera in orders of quadrupedal mammals characteristic of the temperature region (Insectivora, Lagomor- pha, Rodentia, Carnivora, Artiodactyla) and de- grees north latitude shown with the best fit poly- nomial regression line. ALL MAMMALS wn => = WJ oO a ul a wn Ww oO uJ a wn N LATITUDE (a) QUADRUPEDAL MAMMALS 3 20 . z WwW oO [<4 Ww a ” Ww (S) ¥ ”) N LATITUDE (b) 624 ZOOGEOGRAPHY OF NORTH AMERICAN MAMMALS 131 Taste 1. Relationship of species density and topographic relief in quadrats between 40°N and 50°N. Region of high Region of low topographic relief topographic relief % B (> 5000 feet or 1524 m) (< 1000 feet or 304.8 m) Significance Number of quadrats 33 27 Mean Relief 8427 feet (2568 m) 674 feet (205 m) Number of all mammal species 82.9 61 P € .001 Number of quadrupedal mammal species 70.5 52 Pe< 200i Number of Chiroptera species PAS) 9 P<=001 TaBLE 2. Correlation of species density and topographic relief within regions of high and low relief from quadrats between 40°N and 50°N. Region of High Topographic relief (> 5000 feet or 1524 m) Region of low topographic relief (< 1000 feet or 305 m) Correlation Correlation coefficient Significance coefficient Significance Number of all mammal species P< .001 36 Ip ee al Number of quadrupedal mammal species P-<= 001 47 Pe 600 (< 400 mm/yr.) mm/yr.) Significance Number of quadrats 24 34 Mean actual evapotranspiration 637.5 339.7 Mean range of actual evapotranspiration per quadrat | 151.5 P € 001 Number of all mammal species 63.9 79.4 P <€ .001 Number of quadrupedal mammal species 54.2 68.1 P < .001 Number of Chiroptera species 9.8 aS O02. FE ” a WwW = A e ° oO ] [ua WW & QUADRUPEDAL MAMMALS 80 60 40 20 fe) N LATITUDE (b) Fic. 12. Relationship of the ordinal portion of the taxonomic hierarchical diversity measure for (a) all mammals and (b) quadrupedal mam- mals in each quadrat and degrees north latitude shown with the best fit polynomial regression line. quadrupeds (Fig. 14). The values of the family portion of the measure are consis- tently lower than values of the ordinal portion of the measure. Generic level—Only the generic portion of the taxonomic diversity measure shows any marked latitudinal change in value (Fig. 15). The pattern of the values of the generic portion of the measure resembles the pattern of genus density for the total mammal fauna and the quadrupedal mam- mals alone. When the three levels are summed to 133 35 30 é ” ALL MAMMALS “e = = qq we Ww oO a J a = Da az N LATITUDE (a) eee QUADRUPEDAL MAMMALS a = < ioe ire {o) a WW oO = > z N LATITUDE (b) Fic. 13. Relationship of the number of fam- ilies of (a) all mammals and (b) quadrupedal mammals in each quadrat and degrees north lat- itude shown with a linear regression line. form a taxonomic hierarchical diversity measure and this is plotted against lati- tude (Fig. 16), the variations of the or- dinal and family portions essentially can- cel each other except in the far north, and most of the change is due to the generic portion of the diversity measure. DISCUSSION It is possible that the lack of increase in species density of quadrupedal mam- mals is not a latitudinal effect, but is due to the small land area of the isthmus of Central America. To show that this is a general feature of tropical faunas, I gen- erated a species list from Cabrera (1957— 1960) of British Guiana (recommended by Hershkovitz as the best known South Amer- 627 134 ALL MAMMALS FAMILY DIVERSITY 80 60 40 20 fe] N LATITUDE (a) 2 = QUADRUPEDAL MAMMALS = nw ia J = (=) | Fe re N LATITUDE (b) Fic. 14. Relationship of the family portion of the taxonomic hierarchical diversity measure for (a) all mammals and (b) quadrupedal mammals in each quadrat and degrees north latitude shown with the best fit polynomial regression line. ican tropical fauna). The fauna of British Guiana is approximately ten per cent smaller than that of Costa Rica for both quadrupeds and bats. On the basis of this evidence, it seems unlikely that any isth- mus effect is strong enough to explain the results. Unfortunately, it is not possible to compare directly the faunas of Central America and northern South America be- cause the taxonomy of the South American fauna is taxonomically subdivided to a greater extent (some taxa given species status in Cabrera are listed in subspecies in Hall and Kelson, whose taxonomy I have condensed further) and the South American fauna is not as well known. J. W. WILSON > = (77) a WwW > ra wn =) =m uJ (dy) 80 60 40 20 fe) (a) N LATITUDE 2 QUADRUPEDAL MAMMALS > = ao ce lJ = (=) (ep) =) = WW [&) ° (b) Fic. 15. Relationship of the generic portion of the taxonomic hierarchical diversity measure for (a) all mammals and (b) quadrupedal mammals in each quadrat and degrees north latitude shown with the best fit polynomial regression line. N LATITUDE Hierarchical Diversity Measure The measure of taxonomic hierarchical diversity was created to see if species in temperate and tropical faunas were dis- tributed in higher taxonomic categories in a similar manner or if one region contains a fauna where most species are found in a few higher categories while the other has species spread more evenly. Mammal fau- nas, even ones from large quadrats, do not have many species in the same genus; so the diversity measure at the genus level primarily reflects the number of genera. This is similar to using a species diversity 628 ZOOGEOGRAPHY OF NORTH AMERICAN MAMMALS > [ed w 4 [oa J = a = 4 O 2 S ALL MAMMALS a 4 a ud ae 80 60 40 20 (0) N LATITUDE (a) > rE w [os LJ 2 fan) == | aq S) A te oO ce